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Comstock L, Carvalho VR, Lainscsek C, Fallah A, Sejnowski TJ. Transcranial Magnetic Stimulation Facilitates Neural Speech Decoding. Brain Sci 2024; 14:895. [PMID: 39335391 PMCID: PMC11430724 DOI: 10.3390/brainsci14090895] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2024] [Revised: 08/29/2024] [Accepted: 08/30/2024] [Indexed: 09/30/2024] Open
Abstract
Transcranial magnetic stimulation (TMS) has been widely used to study the mechanisms that underlie motor output. Yet, the extent to which TMS acts upon the cortical neurons implicated in volitional motor commands and the focal limitations of TMS remain subject to debate. Previous research links TMS to improved subject performance in behavioral tasks, including a bias in phoneme discrimination. Our study replicates this result, which implies a causal relationship between electro-magnetic stimulation and psychomotor activity, and tests whether TMS-facilitated psychomotor activity recorded via electroencephalography (EEG) may thus serve as a superior input for neural decoding. First, we illustrate that site-specific TMS elicits a double dissociation in discrimination ability for two phoneme categories. Next, we perform a classification analysis on the EEG signals recorded during TMS and find a dissociation between the stimulation site and decoding accuracy that parallels the behavioral results. We observe weak to moderate evidence for the alternative hypothesis in a Bayesian analysis of group means, with more robust results upon stimulation to a brain region governing multiple phoneme features. Overall, task accuracy was a significant predictor of decoding accuracy for phoneme categories (F(1,135) = 11.51, p < 0.0009) and individual phonemes (F(1,119) = 13.56, p < 0.0003), providing new evidence for a causal link between TMS, neural function, and behavior.
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Affiliation(s)
- Lindy Comstock
- Department of Psychiatry & Biobehavioral Sciences, UCLA, Los Angeles, CA 90095, USA
- Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA 90095, USA
| | - Vinícius Rezende Carvalho
- Postgraduate Program in Electrical Engineering, Federal University of Minas Gerais, Belo Horizonte 31270-901, MG, Brazil
| | - Claudia Lainscsek
- Computational Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA
- Institute for Neural Computation, UCSD, San Diego, CA 92093, USA
| | - Aria Fallah
- Department of Neurosurgery, UCLA, Los Angeles, CA 90095, USA
| | - Terrence J. Sejnowski
- Computational Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA 92037, USA
- Institute for Neural Computation, UCSD, San Diego, CA 92093, USA
- Division of Biological Sciences, UCSD, San Diego, CA 92093, USA
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Critzer SS, Bosch TJ, Fercho KA, Scholl JL, Baugh LA. Water and brain function: effects of hydration status on neurostimulation with transcranial magnetic stimulation. J Neurophysiol 2024; 132:791-807. [PMID: 39081213 PMCID: PMC11427052 DOI: 10.1152/jn.00143.2023] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2023] [Revised: 07/15/2024] [Accepted: 07/25/2024] [Indexed: 08/30/2024] Open
Abstract
Neurostimulation/neurorecording are tools to study, diagnose, and treat neurological/psychiatric conditions. Both techniques depend on volume conduction between scalp and excitable brain tissue. Here, we examine how neurostimulation with transcranial magnetic stimulation (TMS) is affected by hydration status, a physiological variable that can influence the volume of fluid spaces/cells, excitability, and cellular/global brain functioning. Normal healthy adult participants (32, 9 males) had common motor TMS measures taken in a repeated-measures design from dehydrated (12-h overnight fast/thirst) and rehydrated (identical dehydration protocol followed by rehydration with 1 L water in 1 h) testing days. The target region was left primary motor cortex hand area. Response at the target muscle was recorded with electromyography. Urinalysis confirmed hydration status. Motor hotspot shifted in half of participants. Motor threshold decreased in rehydration, indicating increased excitability. Even after redosing/relocalizing TMS to the new threshold/hotspot, rehydration still showed evidence of increased excitability: recruitment curve measures generally shifted upward and the glutamate-dependent paired-pulse protocol, short intracortical facilitation (SICF), was increased. Short intracortical inhibition (SICI), long intracortical inhibition (LICI), long intracortical facilitation (LICF), and cortical silent period (CSP) were relatively unaffected. The hydration perturbations were mild/subclinical based on the magnitude/speed and urinalysis. Motor TMS measures showed evidence of expected physiological changes of osmotic challenges. Rehydration showed signs of macroscopic and microscopic volume changes including decreased scalp-cortex distance (brain closer to stimulator) and astrocyte swelling-induced glutamate release. Hydration may be a source of variability affecting any techniques dependent on brain volumes/volume conduction. These concepts are important for researchers/clinicians using such techniques or dealing with the wide variety of disease processes involving water balance.NEW & NOTEWORTHY Hydration status can affect brain volumes and excitability, which should affect techniques dependent on electrical volume conduction, including neurostimulation/recording. We test the previously unknown effects of hydration on neurostimulation with TMS and briefly review relevant physiology of hydration. Rehydration showed lower motor threshold, shifted motor hotspot, and generally larger responses even after compensating for threshold/hotspot changes. This is important for clinical and research applications of neurostimulation/neurorecording and the many clinical disorders related to water balance.
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Affiliation(s)
- Sam S Critzer
- Basic Biomedical Sciences & Center for Brain and Behavior Research, University of South Dakota Sanford School of Medicine, Vermillion, South Dakota, United States
- Department of Psychiatry, University of South Dakota Sanford School of Medicine, Sioux Falls, South Dakota, United States
| | - Taylor J Bosch
- Department of Psychology, University of South Dakota, Vermillion, South Dakota, United States
| | - Kelene A Fercho
- FAA Civil Aerospace Medical Institute, Oklahoma City, Oklahoma, United States
| | - Jamie L Scholl
- Basic Biomedical Sciences & Center for Brain and Behavior Research, University of South Dakota Sanford School of Medicine, Vermillion, South Dakota, United States
| | - Lee A Baugh
- Basic Biomedical Sciences & Center for Brain and Behavior Research, University of South Dakota Sanford School of Medicine, Vermillion, South Dakota, United States
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Beyh A, Howells H, Giampiccolo D, Cancemi D, De Santiago Requejo F, Citro S, Keeble H, Lavrador JP, Bhangoo R, Ashkan K, Dell'Acqua F, Catani M, Vergani F. Connectivity defines the distinctive anatomy and function of the hand-knob area. Brain Commun 2024; 6:fcae261. [PMID: 39239149 PMCID: PMC11375856 DOI: 10.1093/braincomms/fcae261] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/10/2023] [Revised: 05/19/2024] [Accepted: 08/10/2024] [Indexed: 09/07/2024] Open
Abstract
Control of the hand muscles during fine digit movements requires a high level of sensorimotor integration, which relies on a complex network of cortical and subcortical hubs. The components of this network have been extensively studied in human and non-human primates, but discrepancies in the findings obtained from different mapping approaches are difficult to interpret. In this study, we defined the cortical and connectional components of the hand motor network in the same cohort of 20 healthy adults and 3 neurosurgical patients. We used multimodal structural magnetic resonance imaging (including T1-weighted imaging and diffusion tractography), as well as functional magnetic resonance imaging and navigated transcranial magnetic stimulation (nTMS). The motor map obtained from nTMS compared favourably with the one obtained from functional magnetic resonance imaging, both of which overlapped well within the 'hand-knob' region of the precentral gyrus and in an adjacent region of the postcentral gyrus. nTMS stimulation of the precentral and postcentral gyri led to motor-evoked potentials in the hand muscles in all participants, with more responses recorded from precentral stimulations. We also observed that precentral stimulations tended to produce motor-evoked potentials with shorter latencies and higher amplitudes than postcentral stimulations. Tractography showed that the region of maximum overlap between terminations of precentral-postcentral U-shaped association fibres and somatosensory projection tracts colocalizes with the functional motor maps. The relationships between the functional maps, and between them and the tract terminations, were replicated in the patient cohort. Three main conclusions can be drawn from our study. First, the hand-knob region is a reliable anatomical landmark for the functional localization of fine digit movements. Second, its distinctive shape is determined by the convergence of highly myelinated long projection fibres and short U-fibres. Third, the unique role of the hand-knob area is explained by its direct action on the spinal motoneurons and the access to high-order somatosensory information for the online control of fine movements. This network is more developed in the hand region compared to other body parts of the homunculus motor strip, and it may represent an important target for enhancing motor learning during early development.
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Affiliation(s)
- Ahmad Beyh
- NatBrainLab, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London SE5 8AF, UK
- Department of Psychiatry, Brain Health Institute, Rutgers University, Piscataway, NJ 08854, USA
| | - Henrietta Howells
- NatBrainLab, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London SE5 8AF, UK
| | - Davide Giampiccolo
- Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK
- Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK
- Department of Neurosurgery, Institute of Neurosciences, Cleveland Clinic London, London SW1X 7HY, UK
| | - Daniele Cancemi
- NatBrainLab, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London SE5 8AF, UK
| | | | | | - Hannah Keeble
- NatBrainLab, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London SE5 8AF, UK
| | | | - Ranjeev Bhangoo
- Neurosurgical Department, King's College Hospital, London SE5 9RS, UK
| | - Keyoumars Ashkan
- Neurosurgical Department, King's College Hospital, London SE5 9RS, UK
| | - Flavio Dell'Acqua
- NatBrainLab, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London SE5 8AF, UK
| | | | - Francesco Vergani
- Neurosurgical Department, King's College Hospital, London SE5 9RS, UK
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Imazu S, Ikeda S, Toi Y, Sano S, Kanazawa T, Shinosaki K, Tsukuda B, Kita A, Kuroda K, Takahashi S. Real-world outcome of rTMS treatment for depression within the Japanese public health insurance system: Registry data from Kansai TMS network. Asian J Psychiatr 2024; 97:104082. [PMID: 38795414 DOI: 10.1016/j.ajp.2024.104082] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/15/2024] [Revised: 04/30/2024] [Accepted: 05/12/2024] [Indexed: 05/28/2024]
Abstract
This study registered consecutive cases to elucidate the efficacy of rTMS treatment for depression within the Japanese public health insurance system. Of the 102 patients with depression who received rTMS over the left dorsolateral prefrontal cortex, 44 (43.1 %) patients reached remission and 14 (13.7 %) patients did not reach remission but responded to treatment. No serious adverse events occurred. Low baseline HAMD-17 score was associated with remission after rTMS treatment. Favorable outcomes of rTMS treatment were shown in this cohort within the Japanese public insurance system. Our results provide insights into rTMS treatment for depression in real-world clinical setting.
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Affiliation(s)
- Shinichi Imazu
- Department of Neuropsychiatry, Osaka Medical and Pharmaceutical University, 2-7 Daigaku-machi, Takatsuki, Osaka 569-8686, Japan.
| | - Shunichiro Ikeda
- Department of Neuropsychiatry, Kansai Medical University, 10-15 Fumizono-cho, Moriguchi, Osaka 570-8507, Japan
| | - Yuuki Toi
- Department of Psychiatry, Asakayama General Hospital, 3-3-16 Imaike-cho, Sakai, Osaka 590-0018, Japan
| | - Shoko Sano
- Department of Psychiatry, Hannan Hospital, 277 Handa Minamino-cho, Sakai, Osaka 599-8263, Japan
| | - Tetsufumi Kanazawa
- Department of Neuropsychiatry, Osaka Medical and Pharmaceutical University, 2-7 Daigaku-machi, Takatsuki, Osaka 569-8686, Japan
| | - Kazuhiro Shinosaki
- Department of Psychiatry, Asakayama General Hospital, 3-3-16 Imaike-cho, Sakai, Osaka 590-0018, Japan; Clinical Research and Education Center, Asakayama General Hospital, 3-3-16 Imaike-cho, Sakai, Osaka 590-0018, Japan; Osaka Kawasaki Rehabilitation University, 158 Mizuma, Kaizuka, Osaka 597-0104, Japan
| | - Banri Tsukuda
- Department of Neuropsychiatry, Kansai Medical University, 10-15 Fumizono-cho, Moriguchi, Osaka 570-8507, Japan
| | - Akira Kita
- Department of Neuropsychiatry, Wakayama Medical University, 811-1 Kimiidera, Wakayama, Wakayama 641-0012, Japan
| | - Kenji Kuroda
- Department of Psychiatry, Hannan Hospital, 277 Handa Minamino-cho, Sakai, Osaka 599-8263, Japan
| | - Shun Takahashi
- Clinical Research and Education Center, Asakayama General Hospital, 3-3-16 Imaike-cho, Sakai, Osaka 590-0018, Japan; Department of Neuropsychiatry, Wakayama Medical University, 811-1 Kimiidera, Wakayama, Wakayama 641-0012, Japan; Department of Psychiatry, Osaka University Graduate School of Medicine, 2-2 D3 Yamadaoka, Suita, Osaka 565-0871, Japan; Graduate School of Rehabilitation Science, Osaka Metropolitan University, 3-7-30 Habikino, Habikino, Osaka 583-8555, Japan.
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Van Hoornweder S, Geraerts M, Verstraelen S, Nuyts M, Caulfield KA, Meesen R. Differences in scalp-to-cortex tissues across age groups, sexes and brain regions: Implications for neuroimaging and brain stimulation techniques. Neurobiol Aging 2024; 138:45-62. [PMID: 38531217 PMCID: PMC11141186 DOI: 10.1016/j.neurobiolaging.2024.02.011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/06/2023] [Revised: 02/20/2024] [Accepted: 02/21/2024] [Indexed: 03/28/2024]
Abstract
Aging affects the scalp-to-cortex distance (SCD) and the comprising tissues. This is crucial for noninvasive neuroimaging and brain stimulation modalities as they rely on traversing from the scalp to the cortex or vice versa. The specific relationship between aging and these tissues has not been comprehensively investigated. We conducted a study on 250 younger and older adults to examine age-related differences in SCD and its constituent tissues. We identified region-specific differences in tissue thicknesses related to age and sex. Older adults exhibit larger SCD in the frontocentral regions compared to younger adults. Men exhibit greater SCD in the inferior scalp regions, while women show similar-to-greater SCD values in regions closer to the vertex compared to men. Younger adults and men have thicker soft tissue layers, whereas women and older adults exhibit thicker compact bone layers. CSF is considerably thicker in older adults, particularly in men. These findings emphasize the need to consider age, sex, and regional differences when interpreting SCD and its implications for noninvasive neuroimaging and brain stimulation.
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Affiliation(s)
- Sybren Van Hoornweder
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium.
| | - Marc Geraerts
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Stefanie Verstraelen
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Marten Nuyts
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Kevin A Caulfield
- Brain Stimulation Laboratory, Department of Psychiatry, Medical University of South Carolina, Charleston, SC, USA
| | - Raf Meesen
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium; Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium
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Koehler M, Goetz SM. A Closed Formalism for Anatomy-Independent Projection and Optimization of Magnetic Stimulation Coils on Arbitrarily Shaped Surfaces. IEEE Trans Biomed Eng 2024; 71:1745-1755. [PMID: 38206785 DOI: 10.1109/tbme.2024.3350693] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/13/2024]
Abstract
INTRODUCTION Transcranial magnetic stimulation (TMS) is a popular method for the noninvasive stimulation of neurons in the brain. It has become a standard instrument in experimental brain research and has been approved for a range of diagnostic and therapeutic applications. These applications require appropriately shaped coils. Various applications have been established or approved for specific coil designs with their corresponding spatial electric field distributions. However, the specific coil implementation may no longer be appropriate from the perspective of available material and manufacturing opportunities or considering the latest understanding of how to achieve induced electric fields in the head most efficiently. Furthermore, in some cases, field measurements of coils with unknown winding or a user-defined field are available and require an actual implementation. Similar applications exist for magnetic resonance imaging coils. OBJECTIVE This work aims at introducing a complete formalism free from heuristics, iterative optimization, and ad-hoc or manual steps to form practical stimulation coils with individual turns to either equivalently match an existing coil or produce a given field. The target coil can reside on practically any sufficiently large or closed surface adjacent to or around the head. METHODS The method derives an equivalent field through vector projection exploiting the well-known Huygens' and Love's equivalence principle. In contrast to other coil design or optimization approaches recently presented, the procedure is an explicit forward Hilbert-space vector projection or basis change. For demonstration, we map a commercial figure-of-eight coil as one of the most widely used devices and a more intricate coil recently approved clinically for addiction treatment (H4) onto a bent surface close to the head for highest efficiency and lowest field energy. RESULTS The resulting projections are within ≤4% of the target field and reduce the necessary pulse energy by more than 40%.
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Sergiou CS, Tatti E, Romanella SM, Santarnecchi E, Weidema AD, Rassin EG, Franken IH, van Dongen JD. The effect of HD-tDCS on brain oscillations and frontal synchronicity during resting-state EEG in violent offenders with a substance dependence. Int J Clin Health Psychol 2023; 23:100374. [PMID: 36875007 PMCID: PMC9982047 DOI: 10.1016/j.ijchp.2023.100374] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/25/2022] [Accepted: 01/25/2023] [Indexed: 02/24/2023] Open
Abstract
Violence is a major problem in our society and therefore research into the neural underpinnings of aggression has grown exponentially. Although in the past decade the biological underpinnings of aggressive behavior have been examined, research on neural oscillations in violent offenders during resting-state electroencephalography (rsEEG) remains scarce. In this study we aimed to investigate the effect of high-definition transcranial direct current stimulation (HD-tDCS) on frontal theta, alpha and beta frequency power, asymmetrical frontal activity, and frontal synchronicity in violent offenders. Fifty male violent forensic patients diagnosed with a substance dependence were included in a double-blind sham-controlled randomized study. The patients received 20 minutes of HD-tDCS two times a day on five consecutive days. Before and after the intervention, the patients underwent a rsEEG task. Results showed no effect of HD-tDCS on the power in the different frequency bands. Also, no increase in asymmetrical activity was found. However, we found increased synchronicity in frontal regions in the alpha and beta frequency bands indicating enhanced connectivity in frontal brain regions as a result of the HD-tDCS-intervention. This study has enhanced our understanding of the neural underpinnings of aggression and violence, pointing to the importance of alpha and beta frequency bands and their connectivity in frontal brain regions. Although future studies should further investigate the complex neural underpinnings of aggression in different populations and using whole-brain connectivity, it can be suggested with caution, that HD-tDCS could be an innovative method to regain frontal synchronicity in neurorehabilitation.
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Affiliation(s)
- Carmen S. Sergiou
- Department of Psychology, Education and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands
| | - Elisa Tatti
- City College of New York (CUNY) School of Medicine, New York, NY, USA
| | - Sara M. Romanella
- Berenson-Allen Center for Non-Invasive Brain Stimulation, Beth Israel Medical Center, Harvard Medical School, Boston, MA, USA
| | - Emiliano Santarnecchi
- Berenson-Allen Center for Non-Invasive Brain Stimulation, Beth Israel Medical Center, Harvard Medical School, Boston, MA, USA
| | - Alix D. Weidema
- Department of Psychology, Education and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands
| | - Eric G.C Rassin
- Department of Psychology, Education and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands
| | - Ingmar H.A. Franken
- Department of Psychology, Education and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands
| | - Josanne D.M. van Dongen
- Department of Psychology, Education and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands
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Van Hoornweder S, Geraerts M, Verstraelen S, Nuyts M, Caulfield KA, Meesen R. From scalp to cortex, the whole isn't greater than the sum of its parts: introducing GetTissueThickness (GTT) to assess age and sex differences in tissue thicknesses. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2023:2023.04.18.537177. [PMID: 37131842 PMCID: PMC10153183 DOI: 10.1101/2023.04.18.537177] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/04/2023]
Abstract
Noninvasive techniques to record and stimulate the brain rely on passing through the tissues in between the scalp and cortex. Currently, there is no method to obtain detailed information about these scalp-to-cortex distance (SCD) tissues. We introduce GetTissueThickness (GTT), an open-source, automated approach to quantify SCD, and unveil how tissue thicknesses differ across age groups, sexes and brain regions (n = 250). We show that men have larger SCD in lower scalp regions and women have similar-to-larger SCD in regions closer to the vertex, with aging resulting in increased SCD in fronto-central regions. Soft tissue thickness varies by sex and age, with thicker layers and greater age-related decreases in men. Compact and spongy bone thickness also differ across sexes and age groups, with thicker compact bone in women in both age groups and an age-related thickening. Older men generally have the thickest cerebrospinal fluid layer and younger women and men having similar cerebrospinal fluid layers. Aging mostly results in grey matter thinning. Concerning SCD, the whole isn't greater than the sum of its parts. GTT enables rapid quantification of the SCD tissues. The distinctive sensitivity of noninvasive recording and stimulation modalities to different tissues underscores the relevance of GTT.
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Affiliation(s)
- Sybren Van Hoornweder
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Marc Geraerts
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Stefanie Verstraelen
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Marten Nuyts
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
| | - Kevin A. Caulfield
- Brain Stimulation Laboratory, Department of Psychiatry, Medical University of South Carolina, Charleston, SC, USA
| | - Raf Meesen
- REVAL - Rehabilitation Research Center, Faculty of Rehabilitation Sciences, University of Hasselt, Diepenbeek, Belgium
- Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium
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Gogulski J, Ross JM, Talbot A, Cline CC, Donati FL, Munot S, Kim N, Gibbs C, Bastin N, Yang J, Minasi C, Sarkar M, Truong J, Keller CJ. Personalized Repetitive Transcranial Magnetic Stimulation for Depression. BIOLOGICAL PSYCHIATRY. COGNITIVE NEUROSCIENCE AND NEUROIMAGING 2023; 8:351-360. [PMID: 36792455 DOI: 10.1016/j.bpsc.2022.10.006] [Citation(s) in RCA: 9] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/05/2022] [Revised: 10/20/2022] [Accepted: 10/23/2022] [Indexed: 11/06/2022]
Abstract
Personalized treatments are gaining momentum across all fields of medicine. Precision medicine can be applied to neuromodulatory techniques, in which focused brain stimulation treatments such as repetitive transcranial magnetic stimulation (rTMS) modulate brain circuits and alleviate clinical symptoms. rTMS is well tolerated and clinically effective for treatment-resistant depression and other neuropsychiatric disorders. Despite its wide stimulation parameter space (location, angle, pattern, frequency, and intensity can be adjusted), rTMS is currently applied in a one-size-fits-all manner, potentially contributing to its suboptimal clinical response (∼50%). In this review, we examine components of rTMS that can be optimized to account for interindividual variability in neural function and anatomy. We discuss current treatment options for treatment-resistant depression, the neural mechanisms thought to underlie treatment, targeting strategies, stimulation parameter selection, and adaptive closed-loop treatment. We conclude that a better understanding of the wide and modifiable parameter space of rTMS will greatly improve the clinical outcome.
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Affiliation(s)
- Juha Gogulski
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; HUS Diagnostic Center, Clinical Neurophysiology, Clinical Neurosciences, Helsinki University Hospital and University of Helsinki, Helsinki, Finland
| | - Jessica M Ross
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Austin Talbot
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Christopher C Cline
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Francesco L Donati
- Department of Health Sciences, San Paolo Hospital, University of Milan, Milan, Italy
| | - Saachi Munot
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Naryeong Kim
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Ciara Gibbs
- Department of Bioengineering, Imperial College London, London, United Kingdom
| | - Nikita Bastin
- Department of Radiology and Orthopedics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
| | - Jessica Yang
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Christopher Minasi
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Manjima Sarkar
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Jade Truong
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California
| | - Corey J Keller
- Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California; Veterans Affairs Palo Alto Healthcare System, and the Sierra Pacific Mental Illness, Research, Education, and Clinical Center (MIRECC), Palo Alto, California.
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10
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Alawi M, Lee PF, Deng ZD, Goh YK, Croarkin PE. Modelling the differential effects of age on transcranial magnetic stimulation induced electric fields. J Neural Eng 2023; 20. [PMID: 36240726 DOI: 10.1088/1741-2552/ac9a76] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2021] [Accepted: 10/14/2022] [Indexed: 11/11/2022]
Abstract
Objective. The therapeutic application of noninvasive brain stimulation modalities such as transcranial magnetic stimulation (TMS) has expanded in terms of indications and patient populations. Often neurodevelopmental and neurodegenerative changes are not considered in research studies and clinical applications. This study sought to examine TMS dosing across time points in the life cycle.Approach. TMS induced electric fields with a figure-of-eight coil was simulated at left dorsolateral prefrontal cortex regions and taken in vertex as a control region. Realistic magnetic resonance imaging-based head models (N= 48) were concurrently examined in a cross-sectional study of three different age groups (children, adults, and elderlies).Main results. Age had a negative correlation with electric field peaks in white matter, grey matter and cerebrospinal fluid (P< 0.001). Notably, the electric field map in children displayed the widest cortical surface spread of TMS induced electric fields.Significance. Age-related anatomical geometry beneath the coil stimulation site had a significant impact on the TMS induced electric fields for different age groups. Safety considerations for TMS applications and protocols in children are warranted based on the present electric field findings.
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Affiliation(s)
- Mansour Alawi
- Lee Kong Chian Faculty of Engineering & Science, University Tunku Abdul Rahman, Kajang, Malaysia
| | - Poh Foong Lee
- Lee Kong Chian Faculty of Engineering & Science, University Tunku Abdul Rahman, Kajang, Malaysia
| | - Zhi-De Deng
- Noninvasive Neuromodulation Unit, National Institute of Mental Health, NIH, Bethesda, MD, United States of America
| | - Yong Kheng Goh
- Lee Kong Chian Faculty of Engineering & Science, University Tunku Abdul Rahman, Kajang, Malaysia
| | - Paul E Croarkin
- Department of Psychiatry and Psychology, Mayo Clinic, Minnesota, MN, United States of America
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11
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Jiang W, Isenhart R, Sutherland R, Lu Z, Xu H, Pace J, Bonaguidi MA, Lee DJ, Liu CY, Song D. Subthreshold repetitive transcranial magnetic stimulation suppresses ketamine-induced poly population spikes in rat sensorimotor cortex. Front Neurosci 2022; 16:998704. [PMCID: PMC9633989 DOI: 10.3389/fnins.2022.998704] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2022] [Accepted: 09/29/2022] [Indexed: 11/13/2022] Open
Abstract
Cortical oscillations within or across brain regions play fundamental roles in sensory, motor, and memory functions. It can be altered by neuromodulations such as repetitive transcranial magnetic stimulation (rTMS) and pharmacological manipulations such as ketamine. However, the neurobiological basis of the effects of rTMS and ketamine, as well as their interactions, on cortical oscillations is not understood. In this study, we developed and applied a rodent model that enabled simultaneous rTMS treatment, pharmacological manipulations, and invasive electrophysiological recordings, which is difficult in humans. Specifically, a miniaturized C-shaped coil was designed and fabricated to deliver focal subthreshold rTMS above the primary somatosensory (S1) and motor (M1) cortex in rats. Multi-electrode arrays (MEA) were implanted to record local field potentials (LFPs) and single unit activities. A novel form of synchronized activities, poly population spikes (PPS), was discovered as the biomarker of ketamine in LFPs. Brief subthreshold rTMS effectively and reversibly suppressed PPS while increasing the firing rates of single unit activities. These results suggest that ketamine and rTMS have convergent but opposing effects on cortical oscillations and circuits. This highly robust phenomenon has important implications to understanding the neurobiological mechanisms of rTMS and ketamine as well as developing new therapeutic strategies involving both neuromodulation and pharmacological agents.
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Affiliation(s)
- Wenxuan Jiang
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
- *Correspondence: Wenxuan Jiang,
| | - Robert Isenhart
- Rancho Los Amigos National Rehabilitation Center, Downey, CA, United States
- Neurorestoration Center, University of Southern California, Los Angeles, CA, United States
| | - Robert Sutherland
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
| | - Zhouxiao Lu
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
| | - Huijing Xu
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
| | - John Pace
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
| | - Michael A. Bonaguidi
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
- Neurorestoration Center, University of Southern California, Los Angeles, CA, United States
| | - Darrin J. Lee
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
- Rancho Los Amigos National Rehabilitation Center, Downey, CA, United States
- Neurorestoration Center, University of Southern California, Los Angeles, CA, United States
- Department of Neurological Surgery, University of Southern California, Los Angeles, CA, United States
| | - Charles Y. Liu
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
- Rancho Los Amigos National Rehabilitation Center, Downey, CA, United States
- Neurorestoration Center, University of Southern California, Los Angeles, CA, United States
- Department of Neurological Surgery, University of Southern California, Los Angeles, CA, United States
| | - Dong Song
- Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States
- Neurorestoration Center, University of Southern California, Los Angeles, CA, United States
- Dong Song,
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12
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Identifying novel biomarkers with TMS-EEG - Methodological possibilities and challenges. J Neurosci Methods 2022; 377:109631. [PMID: 35623474 DOI: 10.1016/j.jneumeth.2022.109631] [Citation(s) in RCA: 23] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/21/2021] [Revised: 05/09/2022] [Accepted: 05/21/2022] [Indexed: 12/17/2022]
Abstract
Biomarkers are essential for understanding the underlying pathologies in brain disorders and for developing effective treatments. Combined transcranial magnetic stimulation and electroencephalography (TMS-EEG) is an emerging neurophysiological tool that can be used for biomarker development. This method can identify biomarkers associated with the function and dynamics of the inhibitory and excitatory neurotransmitter systems and effective connectivity between brain areas. In this review, we outline the current state of the TMS-EEG biomarker field by summarizing the existing protocols and the possibilities and challenges associated with this methodology.
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13
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Miyazawa A, Kanahara N, Shiko Y, Ozawa Y, Kawasaki Y, Komatsu H, Masumo Y, Nakata Y, Iyo M. The cortical silent period in schizophrenia: A systematic review and meta-analysis focusing on disease stage and antipsychotic medication. J Psychopharmacol 2022; 36:479-488. [PMID: 35475374 DOI: 10.1177/02698811221078751] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/10/2023]
Abstract
BACKGROUND Although numerous studies reported some changes of cortical silent period (CSP), an indicator of gamma-aminobutyric acid (GABA) function in central nervous system, in schizophrenia patients, it has been unknown how the disease stage and antipsychotic medication affect CSP values. METHODS The present study conducted a systematic review of previous literature comparing CSP between schizophrenia patients and healthy subjects, and then performed meta-analysis on the effects of (1) the disease stage and (2) antipsychotics on CSP. RESULTS (1) In the comparison of the disease stage comprising a total of 17 reports, there was no significant difference in CSP between patients under drug-naïve first-episode psychoses and healthy controls, or between patients with antipsychotic medication and healthy controls. (2) In the comparison of the antipsychotic class, patients treated with clozapine were longer in CSP compared to healthy controls. Patients treated with olanzapine/quetiapine or with other type of antipsychotics were not different from healthy controls. Regarding other type of antipsychotics, the iteration analysis after leaving out one literature showed that patients were shorter in CSP than healthy controls. CONCLUSION The results showed that clozapine seems to surely prolong CSP, indicating the enhancement of GABA transmission via GABAB receptors, suggesting the possible relationship between the CSP prolongation by clozapine and its high efficacy in psychopathology. The finding of shorter CSP in patients with other type of antipsychotics was distinct from clozapine/olanzapine/quetiapine, but was difficult to interpret since this group included a variety of transcranial magnetic stimulation (TMS) methodologies and patients' background.
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Affiliation(s)
- Atsuhiro Miyazawa
- Department of Psychiatry, Chiba University Graduate School of Medicine, Chiba, Japan
| | - Nobuhisa Kanahara
- Department of Psychiatry, Chiba University Graduate School of Medicine, Chiba, Japan.,Division of Medical Treatment and Rehabilitation, Center for Forensic Mental Health, Chiba University, Chiba, Japan
| | - Yuki Shiko
- Biostatistics Section, Clinical Research Center, Chiba University Hospital, Chiba, Japan
| | - Yoshihito Ozawa
- Biostatistics Section, Clinical Research Center, Chiba University Hospital, Chiba, Japan
| | - Yohei Kawasaki
- Biostatistics Section, Clinical Research Center, Chiba University Hospital, Chiba, Japan
| | - Hiroshi Komatsu
- Department of Psychiatry, Graduate School of Medicine, Tohoku University, Sendai, Japan
| | - Yuto Masumo
- Department of Psychiatry, Chiba University Graduate School of Medicine, Chiba, Japan
| | - Yusuke Nakata
- Department of Psychiatry, Chiba University Graduate School of Medicine, Chiba, Japan
| | - Masaomi Iyo
- Department of Psychiatry, Chiba University Graduate School of Medicine, Chiba, Japan
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14
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Lien YR, Lin YC, Lin SHN, Lin CP, Chang LH. Frequency-Dependent Effects of Cerebellar Repetitive Transcranial Magnetic Stimulation on Visuomotor Accuracy. Front Neurosci 2022; 16:804027. [PMID: 35368261 PMCID: PMC8971901 DOI: 10.3389/fnins.2022.804027] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2021] [Accepted: 02/14/2022] [Indexed: 12/11/2022] Open
Abstract
The cerebellum plays a critical role in acquiring visuomotor skills. Visuomotor task mastery requires improving both visuomotor accuracy and stability; however, the cerebellum’s contribution to these processes remains unclear. We hypothesized that repetitive transcranial magnetic stimulation (rTMS) of the cerebellum exerts frequency-dependent modulatory effects on both accuracy and stability in subjects performing a visuomotor coordination task (i.e., pursuit rotor task). We recruited 43 healthy volunteers and randomly assigned them to the high-frequency (HF), low-frequency (LF), and sham rTMS groups. We calculated changes in performance of the pursuit rotor task at the highest rotation speed and the minimum distance from target as indices of accuracy. We also calculated the intertrial variability (standard deviations) of time on target and distance from target as indices of stability. Visuomotor accuracy was significantly enhanced in the HF group and disrupted in the LF group compared to the sham group, indicating frequency-dependent effects of rTMS. In contrast, both HF and LF rTMS demonstrated no significant change in visuomotor stability. Surprisingly, our findings demonstrated that the accuracy and stability of visuomotor performance may be differentially influenced by cerebellar rTMS. This suggests that visuomotor accuracy and stability have different underlying neural mechanisms and revealed the possibility of training strategies based on cerebellar neuromodulation.
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Affiliation(s)
- Yun R. Lien
- Institute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, Taiwan
| | - Yi-Cheng Lin
- Institute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, Taiwan
- Taipei Municipal Gan-Dau Hospital, Taipei, Taiwan
| | - Shang-Hua N. Lin
- Institute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, Taiwan
| | - Ching-Po Lin
- Institute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, Taiwan
| | - Li-Hung Chang
- Institute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, Taiwan
- Education Center for Humanities and Social Sciences, National Yang Ming Chiao Tung University, Taipei, Taiwan
- Institute of Philosophy of Mind and Cognition, National Yang Ming Chiao Tung University, Taipei, Taiwan
- *Correspondence: Li-Hung Chang,
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15
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Evaluation and utility of submaximal stimulation intensity in transcranial magnetic stimulation in the standing horse. J Equine Vet Sci 2022; 112:103912. [DOI: 10.1016/j.jevs.2022.103912] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/06/2021] [Revised: 02/14/2022] [Accepted: 02/17/2022] [Indexed: 11/21/2022]
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16
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TMS-EEG responses across the lifespan: Measurement, methods for characterisation and identified responses. J Neurosci Methods 2022; 366:109430. [PMID: 34856320 DOI: 10.1016/j.jneumeth.2021.109430] [Citation(s) in RCA: 21] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/30/2021] [Revised: 11/02/2021] [Accepted: 11/25/2021] [Indexed: 01/29/2023]
Abstract
The combination of transcranial magnetic stimulation (TMS) and electroencephalography (EEG) allows probing of the neurophysiology of any neocortical brain area in vivo with millisecond accuracy. TMS-EEG is particularly unique compared with other available neurophysiological methods, as it can measure the state and dynamics of excitatory and inhibitory systems separately. Because of these capabilities, TMS-EEG responses are sensitive to the brain state, and the responses are influenced by brain maturation and ageing, making TMS-EEG a suitable method to study age-specific pathophysiology. In this review, we outline the TMS-EEG measurement procedure, the existing methods used for characterising TMS-EEG responses and the challenges associated with identifying the responses. We also summarise the findings thus far on how TMS-EEG responses change across the lifespan and the TMS-EEG features that separate typical and atypical brain maturation and ageing. Finally, we give an overview of the gaps in current knowledge to provide directions for future studies.
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17
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Donati FL, Kaskie R, Reis CC, D'Agostino A, Casali AG, Ferrarelli F. Reduced TMS-evoked fast oscillations in the motor cortex predict the severity of positive symptoms in first-episode psychosis. Prog Neuropsychopharmacol Biol Psychiatry 2021; 111:110387. [PMID: 34129889 PMCID: PMC8380703 DOI: 10.1016/j.pnpbp.2021.110387] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/08/2021] [Revised: 06/06/2021] [Accepted: 06/09/2021] [Indexed: 10/21/2022]
Abstract
Accumulating evidence points to neurophysiological abnormalities of the motor cortex in Schizophrenia (SCZ). However, whether these abnormalities represent a core biological feature of psychosis rather than a superimposed neurodegenerative process is yet to be defined, as it is their putative relationship with clinical symptoms. in this study, we used Transcranial Magnetic Stimulation coupled with electroencephalography (TMS-EEG) to probe the intrinsic oscillatory properties of motor (Brodmann Area 4, BA4) and non-motor (posterior parietal, BA7) cortical areas in twenty-three first-episode psychosis (FEP) patients and thirteen age and gender-matched healthy comparison (HC) subjects. Patients underwent clinical evaluation at baseline and six-months after the TMS-EEG session. We found that FEP patients had reduced EEG activity evoked by TMS of the motor cortex in the beta-2 (25-34 Hz) frequency band in a cluster of electrodes overlying BA4, relative to HC participants. Beta-2 deficits in the TMS-evoked EEG response correlated with worse positive psychotic symptoms at baseline and also predicted positive symptoms severity at six-month follow-up assessments. Altogether, these findings indicate that reduced TMS-evoked fast oscillatory activity in the motor cortex is an early neural abnormality that: 1) is present at illness onset; 2) may represent a state marker of psychosis; and 3) could play a role in the development of new tools of outcome prediction in psychotic patients.
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Affiliation(s)
- Francesco Luciano Donati
- Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, United States of America; Department of Health Sciences, University of Milan, Milan, Italy
| | - Rachel Kaskie
- Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, United States of America
| | - Catarina Cardoso Reis
- Institute of Science and Technology, Federal University of São Paulo, São José dos Campos, Brazil
| | | | - Adenauer Girardi Casali
- Institute of Science and Technology, Federal University of São Paulo, São José dos Campos, Brazil
| | - Fabio Ferrarelli
- Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, United States of America.
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18
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Betti S, Fedele M, Castiello U, Sartori L, Budisavljević S. Corticospinal excitability and conductivity are related to the anatomy of the corticospinal tract. Brain Struct Funct 2021; 227:1155-1164. [PMID: 34698904 DOI: 10.1007/s00429-021-02410-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/20/2021] [Accepted: 10/08/2021] [Indexed: 11/30/2022]
Abstract
Probing the brain structure-function relationship is at the heart of modern neuroscientific explorations, enabled by recent advances in brain mapping techniques. This study aimed to explore the anatomical blueprint of corticospinal excitability and shed light on the structure-function relationship within the human motor system. Using diffusion magnetic resonance imaging tractography, based on the spherical deconvolution approach, and transcranial magnetic stimulation (TMS), we show that anatomical inter-individual variability of the corticospinal tract (CST) modulates the corticospinal excitability and conductivity. Our findings show for the first time the relationship between increased corticospinal excitability and conductivity in individuals with a bigger CST (i.e., number of streamlines), as well as increased corticospinal microstructural organization (i.e., fractional anisotropy). These findings can have important implications for the understanding of the neuroanatomical basis of TMS as well as the study of the human motor system in both health and disease.
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Affiliation(s)
- Sonia Betti
- Department of General Psychology, University of Padova, Padova, Italy.
| | - Marta Fedele
- Faculty of Psychology and Educational Sciences, KU Leuven Kulak, Kortrijk, Belgium
| | - Umberto Castiello
- Department of General Psychology, University of Padova, Padova, Italy
| | - Luisa Sartori
- Department of General Psychology, University of Padova, Padova, Italy.,Padova Neuroscience Center, University of Padova, Padova, Italy
| | - Sanja Budisavljević
- Department of General Psychology, University of Padova, Padova, Italy.,School of Medicine, University of St Andrews, St Andrews, UK
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19
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Dyke K, Jackson G, Jackson S. Non-invasive brain stimulation as therapy: systematic review and recommendations with a focus on the treatment of Tourette syndrome. Exp Brain Res 2021; 240:341-363. [PMID: 34643763 PMCID: PMC8858270 DOI: 10.1007/s00221-021-06229-y] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/07/2020] [Accepted: 09/18/2021] [Indexed: 01/06/2023]
Abstract
Tourette syndrome (TS) is a neurodevelopmental condition characterised by tics, which are stereotyped movements and/or vocalisations. Tics often cause difficulties in daily life and many with TS express a desire to reduce and/or gain control over them. No singular effective treatment exists for TS, and while pharmacological and behavioural interventions can be effective, the results are variable, and issues relating to access, availability and side effects can be barriers to treatment. Consequently, over the past decade, there has been increasing interest into the potential benefits of non-invasive brain stimulation (NIBS) approaches. This systematic review highlights work exploring NIBS as a potential treatment for TS. On balance, the results tentatively suggest that multiple sessions of stimulation applied over the supplementary motor area (SMA) may help to reduce tics. However, a number of methodological and theoretical issues limit the strength of this conclusion, with the most problematic being the lack of large-scale sham-controlled studies. In this review, methodological and theoretical issues are discussed, unanswered questions highlighted and suggestions for future work put forward.
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Affiliation(s)
- Katherine Dyke
- School of Psychology, University of Nottingham, Nottingham, UK.
| | - Georgina Jackson
- Institute of Mental Health, School of Medicine, University of Nottingham, Nottingham, UK.,School of Medicine, The University of Nottingham, Nottingham, UK
| | - Stephen Jackson
- School of Psychology, University of Nottingham, Nottingham, UK.,Institute of Mental Health, School of Medicine, University of Nottingham, Nottingham, UK
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20
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Radetz A, Mladenova K, Ciolac D, Gonzalez-Escamilla G, Fleischer V, Ellwardt E, Krämer J, Bittner S, Meuth SG, Muthuraman M, Groppa S. Linking Microstructural Integrity and Motor Cortex Excitability in Multiple Sclerosis. Front Immunol 2021; 12:748357. [PMID: 34712236 PMCID: PMC8546169 DOI: 10.3389/fimmu.2021.748357] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/27/2021] [Accepted: 09/23/2021] [Indexed: 11/15/2022] Open
Abstract
Motor skills are frequently impaired in multiple sclerosis (MS) patients following grey and white matter damage with cortical excitability abnormalities. We applied advanced diffusion imaging with 3T magnetic resonance tomography for neurite orientation dispersion and density imaging (NODDI), as well as diffusion tensor imaging (DTI) in 50 MS patients and 49 age-matched healthy controls to quantify microstructural integrity of the motor system. To assess excitability, we determined resting motor thresholds using non-invasive transcranial magnetic stimulation. As measures of cognitive-motor performance, we conducted neuropsychological assessments including the Nine-Hole Peg Test, Trail Making Test part A and B (TMT-A and TMT-B) and the Symbol Digit Modalities Test (SDMT). Patients were evaluated clinically including assessments with the Expanded Disability Status Scale. A hierarchical regression model revealed that lower neurite density index (NDI) in primary motor cortex, suggestive for axonal loss in the grey matter, predicted higher motor thresholds, i.e. reduced excitability in MS patients (p = .009, adjusted r² = 0.117). Furthermore, lower NDI was indicative of decreased cognitive-motor performance (p = .007, adjusted r² = .142 for TMT-A; p = .009, adjusted r² = .129 for TMT-B; p = .006, adjusted r² = .142 for SDMT). Motor WM tracts of patients were characterized by overlapping clusters of lowered NDI (p <.05, Cohen's d = 0.367) and DTI-based fractional anisotropy (FA) (p <.05, Cohen's d = 0.300), with NDI exclusively detecting a higher amount of abnormally appearing voxels. Further, orientation dispersion index of motor tracts was increased in patients compared to controls, suggesting a decreased fiber coherence (p <.05, Cohen's d = 0.232). This study establishes a link between microstructural characteristics and excitability of neural tissue, as well as cognitive-motor performance in multiple sclerosis. We further demonstrate that the NODDI parameters neurite density index and orientation dispersion index detect a larger amount of abnormally appearing voxels in patients compared to healthy controls, as opposed to the classical DTI parameter FA. Our work outlines the potential for microstructure imaging using advanced biophysical models to forecast excitability alterations in neuroinflammation.
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Affiliation(s)
- Angela Radetz
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Kalina Mladenova
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Dumitru Ciolac
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
- Laboratory of Neurobiology and Medical Genetics, Nicolae Testemițanu State University of Medicine and Pharmacy, Chişinău, Moldova
- Department of Neurology, Institute of Emergency Medicine, Chişinău, Moldova
| | - Gabriel Gonzalez-Escamilla
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Vinzenz Fleischer
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Erik Ellwardt
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Julia Krämer
- Department of Neurology, Institute of Translational Neurology, University Hospital Münster, Münster, Germany
| | - Stefan Bittner
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Sven G. Meuth
- Department of Neurology, Institute of Translational Neurology, University Hospital Münster, Münster, Germany
- Department of Neurology, University Hospital Düsseldorf, Düsseldorf, Germany
| | - Muthuraman Muthuraman
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
| | - Sergiu Groppa
- Neuroimaging and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), Rhine-Main Neuroscience Network (rmn2), University Medical Center of the Johannes Gutenberg-University Mainz, Mainz, Germany
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21
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Kataja J, Soldati M, Matilainen N, Laakso I. A probabilistic transcranial magnetic stimulation localization method. J Neural Eng 2021; 18. [PMID: 34475274 DOI: 10.1088/1741-2552/ac1f2b] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/29/2021] [Accepted: 08/05/2021] [Indexed: 12/15/2022]
Abstract
Objective.Transcranial magnetic stimulation (TMS) can be used to safely and noninvasively activate brain tissue. However, the characteristic parameters of the neuronal activation have been largely unclear. In this work, we propose a novel neuronal activation model and develop a method to infer its parameters from measured motor evoked potential signals.Approach.The connection between neuronal activation due to an induced electric field and a measured motor threshold is modeled. The posterior distribution of the model parameters are inferred from measurement data using Bayes' formula. The measurements are the active motor thresholds obtained with multiple stimulating coil locations, and the parameters of the model are the location, preferred direction of activation, and threshold electric field value of the activation site. The posterior distribution is sampled using a Markov chain Monte Carlo method. We quantify the plausibility of the model by calculating the marginal likelihood of the measured thresholds. The method is validated with synthetic data and applied to motor threshold measurements from the first dorsal interosseus muscle in five healthy participants.Main results.The method produces a probability distribution for the activation location, from which a minimal volume where the activation occurs with 95% probability can be derived. For eight or nine stimulating coil locations, the smallest such a volume obtained was approximately 100 mm3. The 95% probability volume intersected the pre-central gyral crown and the anterior wall of the central sulcus, and the preferred direction was perpendicular to the central sulcus, both findings being consistent with the literature. Furthermore, it was not possible to rule out if the activation occurred either in the white or grey matter. In one participant, two distinct activations sites were found while others exhibited a unique site.Significance.The method is both generic and robust, and it lays a foundation for a framework that enables accurate analysis and characterization of TMS activation mechanisms.
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Affiliation(s)
- Juhani Kataja
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland
| | - Marco Soldati
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland
| | - Noora Matilainen
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland
| | - Ilkka Laakso
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland.,Aalto Neuroimaging, Aalto University, Espoo, Finland
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22
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Mendonça T, Brito R, Luna P, Campêlo M, Shirahige L, Fontes L, Dias R, Piscitelli D, Monte-Silva K. Repetitive transcranial magnetic stimulation on the modulation of cortical and spinal cord excitability in individuals with spinal cord injury. Restor Neurol Neurosci 2021; 39:291-301. [PMID: 34334434 DOI: 10.3233/rnn-211167] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/15/2022]
Abstract
BACKGROUND Repetitive transcranial magnetic stimulation (rTMS) has been applied for modulating cortical excitability and treating spasticity in neurological lesions. However, it is unclear which rTMS frequency is most effective in modulating cortical and spinal excitability in incomplete spinal cord injury (SCI). OBJECTIVE To evaluate electrophysiological and clinical repercussions of rTMS compared to sham stimulation when applied to the primary motor cortex (M1) in individuals with incomplete SCI. METHODS A total of 11 subjects (35±12 years) underwent three experimental sessions of rTMS (10 Hz, 1 Hz and sham stimulation) in a randomized order at 90%intensity of the resting motor threshold and interspersed by a seven-day interval between sessions. The following outcome measures were evaluated: M1 and spinal cord excitability and spasticity in the moments before (baseline), immediately after (T0), 30 (T30) and 60 (T60) minutes after rTMS. M1 excitability was obtained through the motor evoked potential (MEP); spinal cord excitability by the Hoffman reflex (H-reflex) and homosynaptic depression (HD); and spasticity by the modified Ashworth scale (MAS). RESULTS A significant increase in cortical excitability was observed in subjects submitted to 10 Hz rTMS at the T0 moment when compared to sham stimulation (p = 0.008); this increase was also significant at T0 (p = 0.009), T30 (p = 0.005) and T60 (p = 0.005) moments when compared to the baseline condition. No significant differences were observed after the 10 Hz rTMS on spinal excitability or on spasticity. No inter-group differences were detected, or in the time after application of 1 Hz rTMS, or after sham stimulation for any of the assessed outcomes. CONCLUSIONS High-frequency rTMS applied to M1 was able to promote increased cortical excitability in individuals with incomplete SCI for at least 60 minutes; however, it did not modify spinal excitability or spasticity.
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Affiliation(s)
- Thyciane Mendonça
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil
| | - Rodrigo Brito
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil.,NAPeN Network (Núcleo de Assistência e Pesquisa em Neuromodulação), Brazil
| | - Plínio Luna
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil
| | - Mayara Campêlo
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil
| | - Lívia Shirahige
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil.,NAPeN Network (Núcleo de Assistência e Pesquisa em Neuromodulação), Brazil
| | - Luís Fontes
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil
| | - Rebeca Dias
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil
| | - Daniele Piscitelli
- School of Medicine and Surgery, University of Milano-Bicocca, Milano, Italy.,School of Physical and Occupational Therapy, McGill University, Montreal, Canada
| | - Kátia Monte-Silva
- Applied Neuroscience Laboratory, Department of Physical Therapy, Universidade Federal de Pernambuco, UFPE, Recife -PE -Brazil.,NAPeN Network (Núcleo de Assistência e Pesquisa em Neuromodulação), Brazil
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23
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Sollmann N, Krieg SM, Säisänen L, Julkunen P. Mapping of Motor Function with Neuronavigated Transcranial Magnetic Stimulation: A Review on Clinical Application in Brain Tumors and Methods for Ensuring Feasible Accuracy. Brain Sci 2021; 11:brainsci11070897. [PMID: 34356131 PMCID: PMC8305823 DOI: 10.3390/brainsci11070897] [Citation(s) in RCA: 35] [Impact Index Per Article: 8.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/04/2021] [Revised: 06/29/2021] [Accepted: 07/02/2021] [Indexed: 12/15/2022] Open
Abstract
Navigated transcranial magnetic stimulation (nTMS) has developed into a reliable non-invasive clinical and scientific tool over the past decade. Specifically, it has undergone several validating clinical trials that demonstrated high agreement with intraoperative direct electrical stimulation (DES), which paved the way for increasing application for the purpose of motor mapping in patients harboring motor-eloquent intracranial neoplasms. Based on this clinical use case of the technique, in this article we review the evidence for the feasibility of motor mapping and derived models (risk stratification and prediction, nTMS-based fiber tracking, improvement of clinical outcome, and assessment of functional plasticity), and provide collected sets of evidence for the applicability of quantitative mapping with nTMS. In addition, we provide evidence-based demonstrations on factors that ensure methodological feasibility and accuracy of the motor mapping procedure. We demonstrate that selection of the stimulation intensity (SI) for nTMS and spatial density of stimuli are crucial factors for applying motor mapping accurately, while also demonstrating the effect on the motor maps. We conclude that while the application of nTMS motor mapping has been impressively spread over the past decade, there are still variations in the applied protocols and parameters, which could be optimized for the purpose of reliable quantitative mapping.
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Affiliation(s)
- Nico Sollmann
- Department of Diagnostic and Interventional Radiology, University Hospital Ulm, Albert-Einstein-Allee 23, 89081 Ulm, Germany
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Ismaninger Str. 22, 81675 Munich, Germany
- TUM-Neuroimaging Center, Klinikum rechts der Isar, Technical University of Munich, 81675 Munich, Germany;
- Department of Radiology and Biomedical Imaging, University of California San Francisco, 185 Berry Street, San Francisco, CA 94143, USA
- Correspondence:
| | - Sandro M. Krieg
- TUM-Neuroimaging Center, Klinikum rechts der Isar, Technical University of Munich, 81675 Munich, Germany;
- Department of Neurosurgery, School of Medicine, Klinikum rechts der Isar, Technical University of Munich, Ismaninger Str. 22, 81675 Munich, Germany
| | - Laura Säisänen
- Department of Clinical Neurophysiology, Kuopio University Hospital, 70029 Kuopio, Finland; (L.S.); (P.J.)
- Department of Applied Physics, University of Eastern Finland, 70211 Kuopio, Finland
| | - Petro Julkunen
- Department of Clinical Neurophysiology, Kuopio University Hospital, 70029 Kuopio, Finland; (L.S.); (P.J.)
- Department of Applied Physics, University of Eastern Finland, 70211 Kuopio, Finland
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24
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Hare SM, Du X, Adhikari BM, Chen S, Mo C, Summerfelt A, Kvarta MD, Garcia L, Kochunov P, Elliot Hong L. Mapping local and long-distance resting connectivity markers of TMS-related inhibition reduction in schizophrenia. NEUROIMAGE-CLINICAL 2021; 31:102688. [PMID: 33991855 PMCID: PMC8135038 DOI: 10.1016/j.nicl.2021.102688] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 10/31/2020] [Revised: 03/07/2021] [Accepted: 04/26/2021] [Indexed: 11/17/2022]
Abstract
Short interval intracortical inhibition (SICI) is a biomarker for altered motor inhibition in schizophrenia, but the manner in which distant sites influence the inhibitory cortical-effector response remains elusive. Our study investigated local and long-distance resting state functional connectivity (rsFC) markers of SICI in a sample of N = 23 patients with schizophrenia and N = 29 controls. Local functional connectivity was quantified using regional homogeneity (ReHo) analysis and long-range connectivity was estimated using seed-based rsFC analysis. Direct and indirect effects of connectivity measures on SICI were modeled using mediation analysis. Higher SICI ratios (indicating reduced inhibition) in patients were associated with lower ReHo in the right insula. Follow-up rsFC analyses showed that higher SICI scores (indicating reduced inhibition) were associated with reduced connectivity between right insula and hubs of the corticospinal pathway: sensorimotor cortex and basal ganglia. Mediation analysis supported a model in which the direct effect of local insular connectivity strength on SICI is mediated by the interhemispheric connectivity between insula and left sensorimotor cortex. The broader clinical implications of these findings are discussed with emphasis on how these preliminary findings might inform novel interventions designed to restore or improve SICI in schizophrenia and deepen our understanding of motor inhibitory control and impact of abnormal signaling in motor-inhibitory pathways in schizophrenia.
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Affiliation(s)
- Stephanie M Hare
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States.
| | - Xiaoming Du
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Bhim M Adhikari
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Shuo Chen
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Chen Mo
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Ann Summerfelt
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Mark D Kvarta
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Laura Garcia
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Peter Kochunov
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
| | - L Elliot Hong
- Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, United States
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25
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Engelhardt M, Komnenić D, Roth F, Kawelke L, Finke C, Picht T. No Impact of Functional Connectivity of the Motor System on the Resting Motor Threshold: A Replication Study. Front Neurosci 2021; 15:627445. [PMID: 33867916 PMCID: PMC8044353 DOI: 10.3389/fnins.2021.627445] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/09/2020] [Accepted: 02/26/2021] [Indexed: 11/29/2022] Open
Abstract
The physiological mechanisms of corticospinal excitability and factors influencing its measurement with transcranial magnetic stimulation are still poorly understood. A recent study reported an impact of functional connectivity (FC) between the primary motor cortex (M1) and the dorsal premotor cortex (PMd) on the resting motor threshold (RMT) of the dominant hemisphere. We aimed to replicate these findings in a larger sample of 38 healthy right-handed subjects with data from both hemispheres. Resting-state FC was assessed between the M1 and five a priori defined motor-relevant regions on each hemisphere as well as interhemispherically between both primary motor cortices. Following the procedure by the original authors, we included age, cortical gray matter volume, and coil-to-cortex distance (CCD) as further predictors in the analysis. We report replication models for the dominant hemisphere as well as an extension to data from both hemispheres and support the results with Bayes factors. FC between the M1 and the PMd did not explain the variability in the RMT, and we obtained moderate evidence for the absence of this effect. In contrast, CCD could be confirmed as an important predictor with strong evidence. These findings contradict the previously proposed effect, thus questioning the notion of the PMd playing a major role in modifying corticospinal excitability.
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Affiliation(s)
- Melina Engelhardt
- Charité – Universitätsmedizin Berlin, Department of Neurosurgery, Berlin, Germany
- Charité – Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, Germany
| | - Darko Komnenić
- Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany
| | - Fabia Roth
- Charité – Universitätsmedizin Berlin, Department of Neurosurgery, Berlin, Germany
| | - Leona Kawelke
- Charité – Universitätsmedizin Berlin, Department of Neurosurgery, Berlin, Germany
| | - Carsten Finke
- Charité – Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, Germany
- Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany
- Charité – Universitätsmedizin Berlin, Department of Neurology, Berlin, Germany
| | - Thomas Picht
- Charité – Universitätsmedizin Berlin, Department of Neurosurgery, Berlin, Germany
- Charité – Universitätsmedizin Berlin, Einstein Center for Neurosciences, Berlin, Germany
- Cluster of Excellence Matters of Activity, Image Space Material, Humboldt-Universität zu Berlin, Berlin, Germany
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26
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Jiang L, Cui H, Zhang C, Cao X, Gu N, Zhu Y, Wang J, Yang Z, Li C. Repetitive Transcranial Magnetic Stimulation for Improving Cognitive Function in Patients With Mild Cognitive Impairment: A Systematic Review. Front Aging Neurosci 2021; 12:593000. [PMID: 33519418 PMCID: PMC7842279 DOI: 10.3389/fnagi.2020.593000] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2020] [Accepted: 12/02/2020] [Indexed: 12/14/2022] Open
Abstract
Background: Mild cognitive impairment (MCI) is an early stage of Alzheimer's disease. Repetitive transcranial magnetic stimulation (rTMS) has been widely employed in MCI research. However, there is no reliable systematic evidence regarding the effects of rTMS on MCI. The aim of this review was to evaluate the efficacy and safety of rTMS in the treatment of MCI. Methods: A comprehensive literature search of nine electronic databases was performed to identify articles published in English or Chinese before June 20, 2019. The identified articles were screened, data were extracted, and the methodological quality of the included trials was assessed. The meta-analysis was performed using the RevMan 5.3 software. We used the GRADE approach to rate the quality of the evidence. Results: Nine studies comprising 369 patients were included. The meta-analysis showed that rTMS may significantly improve global cognitive function (standardized mean difference [SMD] 2.09, 95% confidence interval [CI] 0.94 to 3.24, p = 0.0004, seven studies, n = 296; low-quality evidence) and memory (SMD 0.44, 95% CI 0.16 to 0.72, p = 0.002, six studies, n = 204; moderate-quality evidence). However, there was no significant improvement in executive function and attention (p > 0.05). Subgroup analyses revealed the following: (1) rTMS targeting the left hemisphere significantly enhanced global cognitive function, while rTMS targeting the bilateral hemispheres significantly enhanced global cognitive function and memory; (2) high-frequency rTMS significantly enhanced global cognitive function and memory; and (3) a high number of treatments ≥20 times could improve global cognitive function and memory. There was no significant difference in dropout rate (p > 0.05) between the rTMS and control groups. However, patients who received rTMS had a higher rate of mild adverse effects (risk ratio 2.03, 95% CI 1.16 to 3.52, p = 0.01, seven studies, n = 317; moderate-quality evidence). Conclusions: rTMS appears to improve global cognitive function and memory in patients with MCI and may have good acceptability and mild adverse effects. Nevertheless, these results should be interpreted cautiously due to the relatively small number of trials, particularly for low-frequency rTMS.
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Affiliation(s)
- Lijuan Jiang
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Huiru Cui
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Caidi Zhang
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Xinyi Cao
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Nannan Gu
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Yikang Zhu
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Jijun Wang
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.,Institute of Psychology and Behavioral Science, Shanghai Jiao Tong University, Shanghai, China.,Center for Excellence in Brain Science and Intelligence Technology (CEBSIT), Chinese Academy of Science, Beijing, China
| | - Zhi Yang
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.,Institute of Psychology and Behavioral Science, Shanghai Jiao Tong University, Shanghai, China.,Brain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, China.,Laboratory of Psychological Heath and Imaging, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Chunbo Li
- Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.,Institute of Psychology and Behavioral Science, Shanghai Jiao Tong University, Shanghai, China.,Center for Excellence in Brain Science and Intelligence Technology (CEBSIT), Chinese Academy of Science, Beijing, China.,Brain Science and Technology Research Center, Shanghai Jiao Tong University, Shanghai, China
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27
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Lu H, Li J, Zhang L, Chan SSM, Lam LCW, for the Open Access Series of Imaging Studies. Dynamic changes of region-specific cortical features and scalp-to-cortex distance: implications for transcranial current stimulation modeling. J Neuroeng Rehabil 2021; 18:2. [PMID: 33397402 PMCID: PMC7784346 DOI: 10.1186/s12984-020-00764-5] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/29/2020] [Accepted: 09/22/2020] [Indexed: 02/02/2023] Open
Abstract
BACKGROUND Transcranial current stimulation in rehabilitation is a fast-growing field featured with computational and biophysical modeling. Cortical features and scalp-to-cortex distance (SCD) are key variables for determining the strength and distribution of the electric field, yet longitudinal studies able to capture these dynamic changes are missing. We sought to investigate and quantify the ageing effect on the morphometry and SCD of left primary motor cortex (M1) and dorsolateral prefrontal cortex (DLPFC) in normal ageing adults and mild cognitive impairment (MCI) converters. METHODS Baseline, 1-year and 3-year follow-up structural magnetic resonance imaging scans from normal ageing adults (n = 32), and MCI converters (n = 22) were drawn from the Open Access Series of Imaging Studies. We quantified the changes of the cortical features and SCDs of left M1 and DLPFC, including grey matter volume, white matter volume, cortical thickness, and folding. Head model was developed to simulate the impact of SCD on the electric field induced by transcranial current stimulation. RESULTS Pronounced ageing effect was found on the SCD of left DLPFC in MCI converters. The SCD change of left DLPFC from baseline to 3-year follow-up demonstrated better performance to discriminate MCI converters from normal ageing adults than the other morphometric measures. The strength of electric field was consequently decreased with SCD in MCI converters. CONCLUSION Ageing has a prominent, but differential effect on the region-specific SCD and cortical features in older adults with cognitive impairments. Our findings suggest that SCD, cortical thickness, and folding of the targeted regions could be used as valuable imaging markers when conducting transcranial brain stimulation in individuals with brain atrophy.
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Affiliation(s)
- Hanna Lu
- Department of Psychiatry, Multi-Centre, The Chinese University of Hong Kong, Tai Po Hospital, Hong Kong SAR, G/F China
- The Affiliated Brain Hospital of Guangzhou Medical University, Guangzhou, China
| | - Jing Li
- Department of Psychiatry, Multi-Centre, The Chinese University of Hong Kong, Tai Po Hospital, Hong Kong SAR, G/F China
| | - Li Zhang
- Department of Mechanical and Automation Engineering, The Chinese University of Hong Kong, Hong Kong SAR, China
| | - Sandra Sau Man Chan
- Department of Psychiatry, Multi-Centre, The Chinese University of Hong Kong, Tai Po Hospital, Hong Kong SAR, G/F China
| | - Linda Chiu Wa Lam
- Department of Psychiatry, Multi-Centre, The Chinese University of Hong Kong, Tai Po Hospital, Hong Kong SAR, G/F China
| | - for the Open Access Series of Imaging Studies
- Department of Psychiatry, Multi-Centre, The Chinese University of Hong Kong, Tai Po Hospital, Hong Kong SAR, G/F China
- The Affiliated Brain Hospital of Guangzhou Medical University, Guangzhou, China
- Department of Mechanical and Automation Engineering, The Chinese University of Hong Kong, Hong Kong SAR, China
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28
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Shah-Basak P, Harvey DY, Parchure S, Faseyitan O, Sacchetti D, Ahmed A, Thiam A, Lohoff FW, Hamilton RH. Brain-Derived Neurotrophic Factor Polymorphism Influences Response to Single-Pulse Transcranial Magnetic Stimulation at Rest. Neuromodulation 2020; 24:S1094-7159(21)06197-3. [PMID: 33090650 PMCID: PMC8032803 DOI: 10.1111/ner.13287] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/03/2020] [Revised: 08/30/2020] [Accepted: 09/02/2020] [Indexed: 12/01/2022]
Abstract
OBJECTIVES The ability of noninvasive brain stimulation to modulate corticospinal excitability and plasticity is influenced by genetic predilections such as the coding for brain-derived neurotrophic factor (BDNF). Otherwise healthy individuals presenting with BDNF Val66Met (Val/Met) polymorphism are less susceptible to changes in excitability in response to repetitive transcranial magnetic stimulation (TMS) and paired associative stimulation paradigms, reflecting reduced neuroplasticity, compared to Val homozygotes (Val/Val). In the current study, we investigated whether BDNF polymorphism influences "baseline" excitability under TMS conditions that are not repetitive or plasticity-inducing. Cross-sectional BDNF levels could predict TMS response more generally because of the ongoing plasticity processes. MATERIALS AND METHODS Forty-five healthy individuals (23 females; age: 25.3 ± 7.0 years) participated in the study, comprising two groups. Motor evoked potentials (MEP) were collected using single-pulse TMS paradigms at fixed stimulation intensities at 110% of the resting motor threshold in one group, and individually-derived intensities based on MEP sizes of 1 mV in the second group. Functional variant Val66Met (rs6265) was genotyped from saliva samples by a technician blinded to the identity of DNA samples. RESULTS Twenty-seven participants (60.0%) were identified with Val/Val, sixteen (35.5%) with Val/Met genotype, and two with Met/Met genotype. MEP amplitudes were significantly diminished in the Val/Met than Val/Val individuals. These results held independent of the single-pulse TMS paradigm of choice (p = 0.017110% group; p = 0.035 1 mV group), age, and scalp-to-coil distances. CONCLUSIONS The findings should be further substantiated in larger-scale studies. If validated, intrinsic differences by BDNF polymorphism status could index response to TMS prior to implementing plasticity-inducing protocols.
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Affiliation(s)
- Priyanka Shah-Basak
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Denise Y. Harvey
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
- Research Department, Moss Rehabilitation Research Institute, 50 Township Line Road, Elkins Park, PA 19027
| | - Shreya Parchure
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Olufunsho Faseyitan
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Daniela Sacchetti
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Ahmed Ahmed
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Abdou Thiam
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
| | - Falk W. Lohoff
- National Institute for Alcohol Abuse and Alcoholism, National Institutes of Health (NIH), 10 Center Drive (10CRC/2-2352), Bethesda, MD 20892-1540
| | - Roy H. Hamilton
- Department of Neurology, University of Pennsylvania, 3710 Hamilton Walk, Philadelphia, PA 19104
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29
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Long-term limb immobilization modulates inhibition-related electrophysiological brain activity. Neuroimage 2020; 218:116911. [DOI: 10.1016/j.neuroimage.2020.116911] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/28/2019] [Revised: 04/28/2020] [Accepted: 04/30/2020] [Indexed: 11/18/2022] Open
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30
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Labruna L, Stark-Inbar A, Breska A, Dabit M, Vanderschelden B, Nitsche MA, Ivry RB. Individual differences in TMS sensitivity influence the efficacy of tDCS in facilitating sensorimotor adaptation. Brain Stimul 2019; 12:992-1000. [PMID: 30930208 PMCID: PMC6592723 DOI: 10.1016/j.brs.2019.03.008] [Citation(s) in RCA: 20] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/05/2018] [Revised: 03/07/2019] [Accepted: 03/07/2019] [Indexed: 11/25/2022] Open
Abstract
BACKGROUND Transcranial direct current stimulation (tDCS) can enhance cognitive function in healthy individuals, with promising applications as a therapeutic intervention. Despite this potential, variability in the efficacy of tDCS has been a considerable concern. OBJECTIVE /Hypothesis: Given that tDCS is always applied at a set intensity, we examined whether individual differences in sensitivity to brain stimulation might be one variable that modulates the efficacy of tDCS in a motor learning task. METHODS In the first part of the experiment, single-pulse transcranial magnetic stimulation (TMS) over primary motor cortex (M1) was used to determine each participant's resting motor threshold (rMT). This measure was used as a proxy of individual sensitivity to brain stimulation. In an experimental group of 28 participants, 2 mA tDCS was then applied during a motor learning task with the anodal electrode positioned over left M1. Another 14 participants received sham stimulation. RESULTS M1-Anodal tDCS facilitated learning relative to participants who received sham stimulation. Of primary interest was a within-group analysis of the experimental group, showing that the rate of learning was positively correlated with rMT: Participants who were more sensitive to brain stimulation as operationalized by our TMS proxy (low rMT), showed faster adaptation. CONCLUSIONS Methodologically, the results indicate that TMS sensitivity can predict tDCS efficacy in a behavioral task, providing insight into one source of variability that may contribute to replication problems with tDCS. Theoretically, the results provide further evidence of a role of sensorimotor cortex in adaptation, with the boost from tDCS observed during acquisition.
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Affiliation(s)
- L Labruna
- Department of Psychology, University of California, 94704, Berkeley, CA, USA; Helen Wills Neuroscience Institute, University of California, 94704, Berkeley, CA, USA.
| | - A Stark-Inbar
- Department of Psychology, University of California, 94704, Berkeley, CA, USA; Helen Wills Neuroscience Institute, University of California, 94704, Berkeley, CA, USA
| | - A Breska
- Department of Psychology, University of California, 94704, Berkeley, CA, USA; Helen Wills Neuroscience Institute, University of California, 94704, Berkeley, CA, USA
| | - M Dabit
- Department of Psychology, University of California, 94704, Berkeley, CA, USA
| | - B Vanderschelden
- Department of Psychology, University of California, 94704, Berkeley, CA, USA
| | - M A Nitsche
- Leibniz Research Center for Working Environment and Human Factors, 44139, Dortmund, Germany
| | - R B Ivry
- Department of Psychology, University of California, 94704, Berkeley, CA, USA; Helen Wills Neuroscience Institute, University of California, 94704, Berkeley, CA, USA
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31
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Rosso C, Lamy JC. Does Resting Motor Threshold Predict Motor Hand Recovery After Stroke? Front Neurol 2018; 9:1020. [PMID: 30555404 PMCID: PMC6281982 DOI: 10.3389/fneur.2018.01020] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/19/2018] [Accepted: 11/12/2018] [Indexed: 12/15/2022] Open
Abstract
Background: Resting Motor threshold (rMT) is one of the measurement obtained by Transcranial Magnetic Stimulation (TMS) that reflects corticospinal excitability. As a functional marker of the corticospinal pathway, the question arises whether rMT is a suitable biomarker for predicting post-stroke upper limb function. To that aim, we conducted a systematic review of relevant studies that investigated the clinical significance of rMT in stroke survivors by using correlations between upper limb motor scores and rMT. Methods: Studies that reported correlations between upper limb motor function and rMT as a measure of corticospinal excitability in distal arm muscle were identified via a literature search in stroke patients. Two authors extracted the data using a home-made specific form. Subgroup analyses were carried out with patients classified with respect to time post-stroke onset (early vs. chronic stage) and stroke location (cortical, subcortical, or cortico-subcortical). Methodological quality of the study was also evaluated by a published checklist. Results: Eighteen studies with 22 groups (n = 508 stroke patients) were included in this systematic review. Mean methodological quality score was 14.75/24. rMT was often correlated with motor function or hand dexterity (n = 15/22, 68%), explaining on average 31% of the variance of the motor score. Moreover, the results did not seem impacted if patients were examined at the early or chronic stages of stroke. Two findings could not be properly interpreted: (i) the fact that the rMT is an independent predictor of motor function as several confounding factors are well-established, and, (ii) whether the stroke location impacts this prediction. Conclusion: Most of the studies found a correlation between rMT and upper limb motor function after stroke. However, it is still unclear if rMT is an independent predictor of upper limb motor function when taking into account for age, time post stroke onset and level of corticospinal tract damage as confounding factors. Clear-cut conclusions could not be drawn at that time but our results suggest that rMT could be a suitable candidate although future investigations are needed. Systematic Review Registration Number: (https://www.crd.york.ac.uk/prospero/): ID 114317.
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Affiliation(s)
- Charlotte Rosso
- Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France.,APHP, Urgences Cérébro-Vasculaires, Hôpital Pitié-Salpêtrière, Paris, France
| | - Jean-Charles Lamy
- Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France
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Soldati M, Mikkonen M, Laakso I, Murakami T, Ugawa Y, Hirata A. A multi-scale computational approach based on TMS experiments for the assessment of electro-stimulation thresholds of the brain at intermediate frequencies. ACTA ACUST UNITED AC 2018; 63:225006. [DOI: 10.1088/1361-6560/aae932] [Citation(s) in RCA: 17] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022]
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Miron JP, Desbeaumes Jodoin V, Montplaisir L, Lespérance P. Significant differences in motor threshold between figure-8 and double-cone coils for repetitive transcranial magnetic stimulation in patients with refractory depression. THE EUROPEAN JOURNAL OF PSYCHIATRY 2018. [DOI: 10.1016/j.ejpsy.2018.06.001] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
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Abstract
Trends in brain stimulation include becoming less invasive, more focal, and more durable with less toxicity. Several of the more interesting new potentially disruptive technologies that are just making their way through basic and sometimes clinical research studies include low-intensity focused ultrasound and temporally interfering electric fields. It is possible, and even likely, that noninvasive brain stimulation may become the dominant form of brain treatments over the next 20 years. The future of brain stimulation therapeutics is bright.
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Affiliation(s)
- Kevin A Caulfield
- Brain Stimulation Laboratory, Medical University of South Carolina, 67 President Street, 502 North, Charleston, SC 29425, USA; Ralph H. Johnson VA Medical Center, 109 Bee Street, Charleston, SC 29401, USA.
| | - Mark S George
- Brain Stimulation Laboratory, Medical University of South Carolina, 67 President Street, 502 North, Charleston, SC 29425, USA; Ralph H. Johnson VA Medical Center, 109 Bee Street, Charleston, SC 29401, USA
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Hanlon CA, Dowdle LT, Henderson JS. Modulating Neural Circuits with Transcranial Magnetic Stimulation: Implications for Addiction Treatment Development. Pharmacol Rev 2018; 70:661-683. [PMID: 29945899 PMCID: PMC6020107 DOI: 10.1124/pr.116.013649] [Citation(s) in RCA: 68] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022] Open
Abstract
Although the last 50 years of clinical and preclinical research have demonstrated that addiction is a brain disease, we still have no neural circuit-based treatments for substance dependence or cue reactivity at large. Now, for the first time, it appears that a noninvasive brain stimulation technique known as transcranial magnetic stimulation (TMS), which is Food and Drug Administration approved to treat depression, may be the first tool available to fill this critical void in addiction treatment development. The goals of this review are to 1) introduce TMS as a tool to induce causal change in behavior, cortical excitability, and frontal-striatal activity; 2) describe repetitive TMS (rTMS) as an interventional tool; 3) provide an overview of the studies that have evaluated rTMS as a therapeutic tool for alcohol and drug use disorders; and 4) outline a conceptual framework for target selection when designing future rTMS clinical trials in substance use disorders. The manuscript concludes with some suggestions for methodological innovation, specifically with regard to combining rTMS with pharmacotherapy as well as cognitive behavioral training paradigms. We have attempted to create a comprehensive manuscript that provides the reader with a basic set of knowledge and an introduction to the primary experimental questions that will likely drive the field of TMS treatment development forward for the next several years.
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Affiliation(s)
- Colleen A Hanlon
- Departments of Psychiatry (C.A.H., L.T.D., J.S.H.) and Neurosciences (C.A.H., L.T.D.), Medical University of South Carolina, Charleston, South Carolina; and Ralph Johnson VA Medical Center, Charleston, South Carolina (C.A.H.)
| | - Logan T Dowdle
- Departments of Psychiatry (C.A.H., L.T.D., J.S.H.) and Neurosciences (C.A.H., L.T.D.), Medical University of South Carolina, Charleston, South Carolina; and Ralph Johnson VA Medical Center, Charleston, South Carolina (C.A.H.)
| | - J Scott Henderson
- Departments of Psychiatry (C.A.H., L.T.D., J.S.H.) and Neurosciences (C.A.H., L.T.D.), Medical University of South Carolina, Charleston, South Carolina; and Ralph Johnson VA Medical Center, Charleston, South Carolina (C.A.H.)
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Chagas AP, Monteiro M, Mazer V, Baltar A, Marques D, Carneiro M, Rodrigues de Araújo MDG, Piscitelli D, Monte-Silva K. Cortical excitability variability: Insights into biological and behavioral characteristics of healthy individuals. J Neurol Sci 2018; 390:172-177. [DOI: 10.1016/j.jns.2018.04.036] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/14/2016] [Revised: 04/13/2018] [Accepted: 04/20/2018] [Indexed: 11/16/2022]
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Mikkonen M, Laakso I, Sumiya M, Koyama S, Hirata A, Tanaka S. TMS Motor Thresholds Correlate With TDCS Electric Field Strengths in Hand Motor Area. Front Neurosci 2018; 12:426. [PMID: 29988501 PMCID: PMC6026630 DOI: 10.3389/fnins.2018.00426] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/13/2017] [Accepted: 07/06/2018] [Indexed: 12/05/2022] Open
Abstract
Transcranial direct current stimulation (TDCS) modulates cortical activity and influences motor and cognitive functions in both healthy and clinical populations. However, there is large inter-individual variability in the responses to TDCS. Computational studies have suggested that inter-individual differences in cranial and brain anatomy may contribute to this variability via creating varying electric fields in the brain. This implies that the electric fields or their strength and orientation should be considered and incorporated when selecting the TDCS dose. Unfortunately, electric field modeling is difficult to perform; thus, a more-robust and practical method of estimating the strength of TDCS electric fields for experimental use is required. As recent studies have revealed a relationship between the sensitivity to TMS and motor cortical TDCS after-effects, the aim of the present study was to investigate whether the resting motor threshold (RMT), a simple measure of transcranial magnetic stimulation (TMS) sensitivity, would be useful for estimating TDCS electric field strengths in the hand area of primary motor cortex (M1). To achieve this, we measured the RMT in 28 subjects. We also obtained magnetic resonance images from each subject to build individual three-dimensional anatomic models, which were used in solving the TDCS and TMS electric fields using the finite element method (FEM). Then, we calculated the correlation between the measured RMT and the modeled TDCS electric fields. We found that the RMT correlated with the TDCS electric fields in hand M1 (R2 = 0.58), but no obvious correlations were identified in regions outside M1. The found correlation was mainly due to a correlation between the TDCS and TMS electric fields, both of which were affected by individual's anatomic features. In conclusion, the RMT could provide a useful tool for estimating cortical electric fields for motor cortical TDCS.
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Affiliation(s)
- Marko Mikkonen
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland
| | - Ilkka Laakso
- Department of Electrical Engineering and Automation, Aalto University, Espoo, Finland
| | - Motofumi Sumiya
- Department of System Neuroscience, National Institute for Physiological Sciences, Okazaki, Japan
| | - Soichiro Koyama
- School of Health Sciences, Faculty of Rehabilitation, Fujita Health University, Toyoake, Japan
| | - Akimasa Hirata
- Department of Computer Science and Engineering, Nagoya Institute of Technology, Nagoya, Japan
| | - Satoshi Tanaka
- Laboratory of Psychology, Hamamatsu University School of Medicine, Hamamatsu, Japan
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Bruno V, Fossataro C, Garbarini F. Report of seizure induced by 10 Hz rTMS over M1. Brain Stimul 2018; 11:454-455. [DOI: 10.1016/j.brs.2017.11.003] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/14/2017] [Revised: 11/01/2017] [Accepted: 11/05/2017] [Indexed: 11/16/2022] Open
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Kaskie RE, Ferrarelli F. Investigating the neurobiology of schizophrenia and other major psychiatric disorders with Transcranial Magnetic Stimulation. Schizophr Res 2018; 192:30-38. [PMID: 28478887 DOI: 10.1016/j.schres.2017.04.045] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/26/2016] [Revised: 04/24/2017] [Accepted: 04/26/2017] [Indexed: 11/16/2022]
Abstract
Characterizing the neurobiology of schizophrenia and other major psychiatric disorders is one of the main challenges of the current research in psychiatry. The availability of Transcranial Magnetic Stimulation (TMS) allows to directly probe virtually any cortical areas, thus providing a unique way to assess the neurophysiological properties of cortical neurons. This article presents a review of studies employing TMS in combination with Motor Evoked Potentials (TMS/MEPs) and high density Electroencephalogram (TMS/hd-EEG) in schizophrenia and other major psychiatric disorders. Studies were identified by conducting a PubMed search using the following search item: "transcranial magnetic stimulation and (Schizophrenia or OCD or MDD or ADHD)". Studies that utilized TMS/MEP and/or TMS/hd-EEG measures to characterize cortical excitability, inhibition, oscillatory activity, and/or connectivity in psychiatric patients were selected. Across disorders, patients displayed a pattern of reduced cortical inhibition, and to a lesser extent increased excitability, in the motor cortex, which was most consistently established in Schizophrenia. Furthermore, psychiatric patients showed abnormalities in a number of TMS-evoked EEG oscillations, which was most prominent in the prefrontal cortex of Schizophrenia relative to healthy comparison subjects. Overall, results from this review point to significant impairments in cortical excitability, inhibition, and oscillatory activity, especially in frontal areas, in several major psychiatric disorders. Building on these findings, future studies employing TMS-based experimental paradigms may help elucidating the neurobiology of these psychiatric disorders, and may assess the contribution of TMS-related measures in monitoring and possibly maximizing the effectiveness of treatment interventions in psychiatric populations.
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40
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Valero-Cabré A, Amengual JL, Stengel C, Pascual-Leone A, Coubard OA. Transcranial magnetic stimulation in basic and clinical neuroscience: A comprehensive review of fundamental principles and novel insights. Neurosci Biobehav Rev 2017; 83:381-404. [DOI: 10.1016/j.neubiorev.2017.10.006] [Citation(s) in RCA: 190] [Impact Index Per Article: 23.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/07/2017] [Revised: 09/29/2017] [Accepted: 10/06/2017] [Indexed: 01/13/2023]
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Notzon S, Vennewald N, Gajewska A, Klahn AL, Diemer J, Winter B, Fohrbeck I, Arolt V, Pauli P, Domschke K, Zwanzger P. Is prepulse modification altered by continuous theta burst stimulation? DAT1 genotype and motor threshold interact on prepulse modification following brain stimulation. Eur Arch Psychiatry Clin Neurosci 2017; 267:767-779. [PMID: 28337537 DOI: 10.1007/s00406-017-0786-x] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/23/2016] [Accepted: 03/13/2017] [Indexed: 12/14/2022]
Abstract
Previous studies suggest an inhibitory top-down control of the amygdala by the prefrontal cortex (PFC). Both brain regions play a role in the modulation of prepulse modification (PPM) of the acoustic startle response by a pre-stimulus. Repetitive transcranial magnetic stimulation (rTMS) can modulate the activity of the PFC and might thus affect PPM. This study tested the effect of inhibitory rTMS on PPM accounting for a genetic variant of the dopamine transporter gene (DAT1). Healthy participants (N = 102) were stimulated with continuous theta burst stimulation (cTBS, an intense form of inhibitory rTMS) or sham treatment over the right PFC. Afterwards, during continuous presentation of a background white noise a louder noise burst was presented either alone (control startle) or preceded by a prepulse. Participants were genotyped for a DAT1 variable number tandem repeat (VNTR) polymorphism. Two succeeding sessions of cTBS over the right PFC (2 × 600 stimuli with a time lag of 15 min) attenuated averaged prepulse inhibition (PPI) in participants with a high resting motor threshold. An attenuation of PPI induced by prepulses with great distances to the pulse (480, 2000 ms) was observed following active cTBS in participants that were homozygous carriers of the 10-repeat-allele of the DAT1 genotype and had a high resting motor threshold. Our results confirm the importance of the prefrontal cortex for the modulation of PPM. The effects were observed in participants with a high resting motor threshold only, probably because they received a higher dose of cTBS. The effects in homozygous carriers of the DAT1 10-repeat allele confirm the relevance of dopamine for PPM. Conducting an exploratory study we decided against the use of a correction for multiple testing.
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Affiliation(s)
- S Notzon
- Department of Psychiatry and Psychotherapy, University of Münster, Albert-Schweitzer-Campus 1, Gebäude A9, 48149, Münster, Germany.
| | - N Vennewald
- School of Health, Münster University of Applied Sciences, Leonardo Campus 8, 48149, Münster, Germany
| | - A Gajewska
- Department of Psychiatry, Psychosomatics and Psychotherapy, University of Würzburg, Margarete-Höppel-Platz 1, 97080, Würzburg, Germany
| | - A L Klahn
- Department of Psychiatry and Psychotherapy, University of Münster, Albert-Schweitzer-Campus 1, Gebäude A9, 48149, Münster, Germany
| | - J Diemer
- kbo-Inn-Salzach-Hospital, Gabersee 7, 83512, Wasserburg am Inn, Germany
| | - B Winter
- Catholic University of Applied Sciences North Rhine-Westphalia, Münster, Piusallee 89, 48147, Münster, Germany
| | - I Fohrbeck
- Department of Psychiatry and Psychotherapy, University of Münster, Albert-Schweitzer-Campus 1, Gebäude A9, 48149, Münster, Germany
| | - V Arolt
- Department of Psychiatry and Psychotherapy, University of Münster, Albert-Schweitzer-Campus 1, Gebäude A9, 48149, Münster, Germany
| | - P Pauli
- Department of Biological Psychology, Clinical Psychology and Psychotherapy, University of Würzburg, Marcusstraße 9-11, 97070, Würzburg, Germany
| | - K Domschke
- Department of Psychiatry, Psychosomatics and Psychotherapy, University of Würzburg, Margarete-Höppel-Platz 1, 97080, Würzburg, Germany
- Department of Psychiatry and Psychotherapy, University of Freiburg, Hauptstrasse 5, 79104, Freiburg, Germany
| | - P Zwanzger
- Department of Psychiatry and Psychotherapy, University of Münster, Albert-Schweitzer-Campus 1, Gebäude A9, 48149, Münster, Germany
- kbo-Inn-Salzach-Hospital, Gabersee 7, 83512, Wasserburg am Inn, Germany
- Department of Psychiatry und Psychotherapy, Ludwig Maximilians University, Munich, Germany
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Bruno V, Fossataro C, Bolognini N, Zigiotto L, Vallar G, Berti A, Garbarini F. The role of premotor and parietal cortex during monitoring of involuntary movement: A combined TMS and tDCS study. Cortex 2017; 96:83-94. [DOI: 10.1016/j.cortex.2017.09.001] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2017] [Revised: 08/14/2017] [Accepted: 09/01/2017] [Indexed: 10/18/2022]
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Automatized set-up procedure for transcranial magnetic stimulation protocols. Neuroimage 2017; 153:307-318. [DOI: 10.1016/j.neuroimage.2017.04.001] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/16/2016] [Revised: 02/03/2017] [Accepted: 04/01/2017] [Indexed: 12/15/2022] Open
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Rosso C, Perlbarg V, Valabregue R, Obadia M, Kemlin-Méchin C, Moulton E, Leder S, Meunier S, Lamy JC. Anatomical and functional correlates of cortical motor threshold of the dominant hand. Brain Stimul 2017; 10:952-958. [PMID: 28551318 DOI: 10.1016/j.brs.2017.05.005] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/13/2017] [Revised: 05/04/2017] [Accepted: 05/15/2017] [Indexed: 10/19/2022] Open
Abstract
BACKGROUND Resting Motor threshold (rMT) provides information about cortical motor excitability. Interestingly, the influences of the structural or functional variability of the motor system on the rMT inter-individual variability have been poorly investigated. OBJECTIVE/HYPOTHESIS To investigate relationships between rMT and measures of brain structures and function of the motor system. The hypothesis is that cortical excitability not only depends on the primary motor cortex (M1) but also on the integration of information originating from its vicinity such as premotor (PMd and SMA) and post-central (S1) cortices. METHODS We measured brain structures, including grey and white matter properties (cortical volume and fiber coherence respectively), and functional interaction (resting-state functional connectivity-FC) in areas contributing to the corticospinal tract axons, i. e, M1, S1, SMA and PMd in the dominant hemisphere of 21 healthy subjects. RESULTS The rMT was inversely correlated with the FC between PMd and M1 (r = -0.496, 95%CI: -0.764; -0.081; p = 0.02) and the grey matter volume of the dominant hemisphere (r = -0.463, 95%CI: -0.746; -0.039; p = 0.03). The multiple regression analysis model retained the FC between M1 and PMd (coefficient: -25 ± 9) as well as the grey matter volume of the dominant hemisphere (coefficient: -0.15 ± 0.06) explaining 44% of the variance of the rMT (p: 0.005). When adding age and coil-to-cortex distance, two factors known to influence rMT, the model reached a R2 of 75% (p: 0.0001). CONCLUSIONS These results underline the major role of the PMd and the cortico-cortical connections toward M1 in the excitation of the corticospinal fibers likely through trans-synaptic pathways.
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Affiliation(s)
- Charlotte Rosso
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France; AP-HP, Urgences Cérébro-Vasculaires, Hôpital Pitié-Salpêtrière, F-75013, Paris, France.
| | - Vincent Perlbarg
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France; Sorbonne Universités, UPMC Univ Paris 06, CNRS, INSERM, Laboratoire d'imagerie biomédicale (LIB), F-75013, Paris, France; Bioinformatics and Biostatistics Core Facility, iCONICS, IHU-A-ICM, Institut du Cerveau et de la Moelle épinière, Paris, France
| | - Romain Valabregue
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France; Centre de Neuro-imagerie de Recherche, CENIR, F-75013, Paris, France
| | - Mickaël Obadia
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France; AP-HP, Urgences Cérébro-Vasculaires, Hôpital Pitié-Salpêtrière, F-75013, Paris, France
| | - Claire Kemlin-Méchin
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France
| | - Eric Moulton
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France
| | - Sara Leder
- AP-HP, Urgences Cérébro-Vasculaires, Hôpital Pitié-Salpêtrière, F-75013, Paris, France
| | - Sabine Meunier
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France
| | - Jean-Charles Lamy
- Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, F-75013, Paris, France; Centre de Neuro-imagerie de Recherche, CENIR, F-75013, Paris, France
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Määttä S, Könönen M, Kallioniemi E, Lakka T, Lintu N, Lindi V, Ferreri F, Ponzo D, Säisänen L. Development of cortical motor circuits between childhood and adulthood: A navigated TMS-HdEEG study. Hum Brain Mapp 2017; 38:2599-2615. [PMID: 28218489 PMCID: PMC6866783 DOI: 10.1002/hbm.23545] [Citation(s) in RCA: 32] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/13/2016] [Revised: 02/08/2017] [Accepted: 02/09/2017] [Indexed: 12/18/2022] Open
Abstract
Motor functions improve during childhood and adolescence, but little is still known about the development of cortical motor circuits during early life. To elucidate the neurophysiological hallmarks of motor cortex development, we investigated the differences in motor cortical excitability and connectivity between healthy children, adolescents, and adults by means of navigated suprathreshold motor cortex transcranial magnetic stimulation (TMS) combined with high-density electroencephalography (EEG). We demonstrated that with development, the excitability of the motor system increases, the TMS-evoked EEG waveform increases in complexity, the magnitude of induced activation decreases, and signal spreading increases. Furthermore, the phase of the oscillatory response to TMS becomes less consistent with age. These changes parallel an improvement in manual dexterity and may reflect developmental changes in functional connectivity. Hum Brain Mapp 38:2599-2615, 2017. © 2017 Wiley Periodicals, Inc.
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Affiliation(s)
- Sara Määttä
- Department of Clinical NeurophysiologyInstitute of Clinical Medicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
- Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
| | - Mervi Könönen
- Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
- Department of Clinical RadiologyKuopio University HospitalKuopioFinland
| | - Elisa Kallioniemi
- Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
- Department of Applied PhysicsUniversity of Eastern FinlandKuopioFinland
| | - Timo Lakka
- Institute of Biomedicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
- Department of Clinical Physiology and Nuclear MedicineKuopio University HospitalKuopioFinland
- Kuopio Research Institute of Exercise MedicineKuopioFinland
| | - Niina Lintu
- Institute of Biomedicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
| | - Virpi Lindi
- Institute of Biomedicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
| | - Florinda Ferreri
- Department of Clinical NeurophysiologyInstitute of Clinical Medicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
- Department of NeurologyUniversity Campus BiomedicoRomeItaly
| | - David Ponzo
- Department of NeurologyUniversity Campus BiomedicoRomeItaly
| | - Laura Säisänen
- Department of Clinical NeurophysiologyInstitute of Clinical Medicine, Faculty of Health Sciences, University of Eastern FinlandKuopioFinland
- Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
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Ustohal L, Mayerova M, Hublova V, Prikrylova Kucerova H, Ceskova E, Kasparek T. Risperidone increases the cortical silent period in drug-naive patients with first-episode schizophrenia: A transcranial magnetic stimulation study. J Psychopharmacol 2017; 31:500-504. [PMID: 27527735 DOI: 10.1177/0269881116662650] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/15/2022]
Abstract
OBJECTIVES Schizophrenia is accompanied by impaired cortical inhibition, as measured by several markers including the cortical silent period (CSP). It is thought that CSP measures gamma-aminobutyric acid receptors B (GABAB) mediated inhibitory activity. But the mutual roles of schizophrenia as a disease and the drugs used for the treatment of psychosis on GABA mediated neurotransmission are not clear. METHODS We recruited 13 drug-naive patients with first-episode schizophrenia. We used transcranial magnetic stimulation to assess CSP prior to initiating risperidone monotherapy and again four weeks later. At the same time, we rated the severity of psychopathology using the Positive and Negative Syndrome Scale (PANSS). RESULTS We obtained data from 12 patients who showed a significant increase in CSP, from 134.20±41.81 ms to 162.95±61.98 ms ( p=0.041; Cohen's d=0.544). After the treatment, the PANSS total score was significantly lower, as were the individual subscores ( p<0.05). However, no correlation was found between ΔCSP and ΔPANSS. CONCLUSION Our study in patients with first-episode schizophrenia demonstrated an association between risperidone monotherapy and an increase in GABAB mediated inhibitory neurotransmission.
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Affiliation(s)
- Libor Ustohal
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic.,2 Central European Institute of Technology, Masaryk University, Brno, Czech Republic
| | - Michaela Mayerova
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic.,2 Central European Institute of Technology, Masaryk University, Brno, Czech Republic
| | - Veronika Hublova
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic
| | - Hana Prikrylova Kucerova
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic
| | - Eva Ceskova
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic.,2 Central European Institute of Technology, Masaryk University, Brno, Czech Republic
| | - Tomas Kasparek
- 1 Department of Psychiatry, Medical Faculty of Masaryk University and University Hospital Brno, Brno, Czech Republic.,2 Central European Institute of Technology, Masaryk University, Brno, Czech Republic
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Strube W, Bunse T, Nitsche MA, Nikolaeva A, Palm U, Padberg F, Falkai P, Hasan A. Bidirectional variability in motor cortex excitability modulation following 1 mA transcranial direct current stimulation in healthy participants. Physiol Rep 2017; 4:4/15/e12884. [PMID: 27495298 PMCID: PMC4985549 DOI: 10.14814/phy2.12884] [Citation(s) in RCA: 54] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/13/2016] [Accepted: 07/15/2016] [Indexed: 11/24/2022] Open
Abstract
Due to the high interindividual response variability following transcranial direct current stimulation (tDCS), it is apparent that further research of the long‐lasting effects of the stimulation technique is required. We aimed to investigate interindividual variability following anodal tDCS and cathodal tDCS in a large‐scale prospective cross‐over study. Motor cortex physiology measurements were obtained using transcranial magnetic stimulation (TMS) in 59 healthy participants comparing motor‐evoked potential (MEP) magnitudes following two tDCS paradigms: 1 mA anodal tDCS for 13 min and 1 mA cathodal tDCS for 9 min. Analysis compared MEP changes over time for both polarities. Additionally, we applied hierarchical cluster analysis to assess the dynamics of poststimulation changes. Overall, anodal tDCS resulted in a significant increase in corticospinal excitability lasting for 40 min poststimulation, whereas cathodal tDCS did not alter corticospinal excitability. Cluster analysis revealed for cathodal tDCS both a cluster showing significant stable MEP reduction and a second cluster displaying MEP increase over time. Two diametrical clusters were also found for anodal tDCS. Regardless of polarity, individuals with MEP increase following stimulation showed steeper cortical recruitment curves compared to the clusters with decreased MEP magnitudes. The observed findings confirm a bidirectional modulation of corticospinal excitability following 1 mA tDCS in separate subgroups and the relationship to cortical recruitment.
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Affiliation(s)
- Wolfgang Strube
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Tilmann Bunse
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Michael A Nitsche
- Department of Neurology, University Medical Hospital Bergmannsheil, Bochum, Germany Leibniz Research Centre for Working Environment and Human Factors TU Dortmund, Dortmund, Germany
| | - Alexandra Nikolaeva
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Ulrich Palm
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Frank Padberg
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Peter Falkai
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
| | - Alkomiet Hasan
- Department of Psychiatry and Psychotherapy, Ludwig Maximillian University, Munich, Germany
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Jamil A, Batsikadze G, Kuo H, Labruna L, Hasan A, Paulus W, Nitsche MA. Systematic evaluation of the impact of stimulation intensity on neuroplastic after-effects induced by transcranial direct current stimulation. J Physiol 2017; 595:1273-1288. [PMID: 27723104 PMCID: PMC5309387 DOI: 10.1113/jp272738] [Citation(s) in RCA: 281] [Impact Index Per Article: 35.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2016] [Accepted: 10/04/2016] [Indexed: 11/08/2022] Open
Abstract
KEY POINTS Applications of transcranial direct current stimulation to modulate human neuroplasticity have increased in research and clinical settings. However, the need for longer-lasting effects, combined with marked inter-individual variability, necessitates a deeper understanding of the relationship between stimulation parameters and physiological effects. We systematically investigated the full DC intensity range (0.5-2.0 mA) for both anodal and cathodal tDCS in a sham-controlled repeated measures design, monitoring changes in motor-cortical excitability via transcranial magnetic stimulation up to 2 h after stimulation. For both tDCS polarities, the excitability after-effects did not linearly correlate with increasing DC intensity; effects of lower intensities (0.5, 1.0 mA) showed equal, if not greater effects in motor-cortical excitability. Further, while intra-individual responses showed good reliability, inter-individual sensitivity to TMS accounted for a modest percentage of the variance in the early after-effects of 1.0 mA anodal tDCS, which may be of practical relevance for future optimizations. ABSTRACT Contemporary non-invasive neuromodulatory techniques, such as transcranial direct current stimulation (tDCS), have shown promising potential in both restituting impairments in cortical physiology in clinical settings, as well as modulating cognitive abilities in the healthy population. However, neuroplastic after-effects of tDCS are highly dependent on stimulation parameters, relatively short lasting, and not expectedly uniform between individuals. The present study systematically investigates the full range of current intensity between 0.5 and 2.0 mA on left primary motor cortex (M1) plasticity, as well as the impact of individual-level covariates on explaining inter-individual variability. Thirty-eight healthy subjects were divided into groups of anodal and cathodal tDCS. Five DC intensities (sham, 0.5, 1.0, 1.5 and 2.0 mA) were investigated in separate sessions. Using transcranial magnetic stimulation (TMS), 25 motor-evoked potentials (MEPs) were recorded before, and 10 time points up to 2 h following 15 min of tDCS. Repeated-measures ANOVAs indicated a main effect of intensity for both anodal and cathodal tDCS. With anodal tDCS, all active intensities resulted in equivalent facilitatory effects relative to sham while for cathodal tDCS, only 1.0 mA resulted in sustained excitability diminution. An additional experiment conducted to assess intra-individual variability revealed generally good reliability of 1.0 mA anodal tDCS (ICC(2,1) = 0.74 over the first 30 min). A post hoc analysis to discern sources of inter-individual variability confirmed a previous finding in which individual TMS SI1mV (stimulus intensity for 1 mV MEP amplitude) sensitivity correlated negatively with 1.0 mA anodal tDCS effects on excitability. Our study thus provides further insights on the extent of non-linear intensity-dependent neuroplastic after-effects of anodal and cathodal tDCS.
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Affiliation(s)
- Asif Jamil
- Department of Clinical NeurophysiologyUniversity Medical Center, University of Göttingen37075GöttingenGermany
- Leibniz Research Centre for Working Environment and Human Factors44139DortmundGermany
| | - Giorgi Batsikadze
- Department of Clinical NeurophysiologyUniversity Medical Center, University of Göttingen37075GöttingenGermany
| | - Hsiao‐I. Kuo
- Department of Clinical NeurophysiologyUniversity Medical Center, University of Göttingen37075GöttingenGermany
- Leibniz Research Centre for Working Environment and Human Factors44139DortmundGermany
| | - Ludovica Labruna
- Department of PsychologyUniversity of CaliforniaBerkeleyCA94720USA
| | - Alkomiet Hasan
- Department of Psychiatry and PsychotherapyKlinikum der Universität München80336MünchenGermany
| | - Walter Paulus
- Department of Clinical NeurophysiologyUniversity Medical Center, University of Göttingen37075GöttingenGermany
| | - Michael A. Nitsche
- Leibniz Research Centre for Working Environment and Human Factors44139DortmundGermany
- University Medical Hospital Bergmannsheil44789BochumGermany
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Individual Differences in Resting Corticospinal Excitability Are Correlated with Reaction Time and GABA Content in Motor Cortex. J Neurosci 2017; 37:2686-2696. [PMID: 28179557 DOI: 10.1523/jneurosci.3129-16.2017] [Citation(s) in RCA: 45] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/07/2016] [Revised: 01/04/2017] [Accepted: 01/31/2017] [Indexed: 01/14/2023] Open
Abstract
Individuals differ in the intrinsic excitability of their corticospinal pathways and, perhaps more generally, their entire nervous system. At present, we have little understanding of the mechanisms underlying these differences and how variation in intrinsic excitability relates to behavior. Here, we examined the relationship between individual differences in intrinsic corticospinal excitability, local cortical GABA levels, and reaction time (RT) in a group of 20 healthy human adults. We measured corticospinal excitability at rest with transcranial magnetic stimulation, local concentrations of basal GABA with magnetic resonance spectroscopy, and RT with a behavioral task. All measurements were repeated in two separate sessions, and tests of reliability confirmed the presence of stable individual differences. There was a negative correlation between corticospinal excitability and RT, such that larger motor-evoked potentials (MEPs) measured at rest were associated with faster RTs. Interestingly, larger MEPs were associated with higher levels of GABA in M1, but not in three other cortical regions. Together, these results suggest that individuals with more excitable corticospinal pathways are faster to initiate planned responses and have higher levels of GABA within M1, possibly to compensate for a more excitable motor system.SIGNIFICANCE STATEMENT This study brings together physiological, behavioral, and neurochemical evidence to examine variability in the excitability of the human motor system. Previous work has focused on state-based factors (e.g., preparedness, uncertainty), with little attention given to the influence of inherent stable characteristics. Here, we examined how the excitability of the motor system relates to reaction time and the regional content of the inhibitory neurotransmitter GABA. Importantly, motor pathway excitability and GABA concentrations were measured at rest, outside a task context, providing assays of intrinsic properties of the individuals. Individuals with more excitable motor pathways had faster reaction times and, paradoxically, higher concentrations of GABA. We propose that greater GABA capacity in the motor cortex counteracts an intrinsically more excitable motor system.
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Immediate Effects of Repetitive Magnetic Stimulation on Single Cortical Pyramidal Neurons. PLoS One 2017; 12:e0170528. [PMID: 28114421 PMCID: PMC5256952 DOI: 10.1371/journal.pone.0170528] [Citation(s) in RCA: 48] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/25/2016] [Accepted: 12/18/2016] [Indexed: 11/19/2022] Open
Abstract
Repetitive Transcranial Magnetic Stimulation (rTMS) has been successfully used as a non-invasive therapeutic intervention for several neurological disorders in the clinic as well as an investigative tool for basic neuroscience. rTMS has been shown to induce long-term changes in neuronal circuits in vivo. Such long-term effects of rTMS have been investigated using behavioral, imaging, electrophysiological, and molecular approaches, but there is limited understanding of the immediate effects of TMS on neurons. We investigated the immediate effects of high frequency (20 Hz) rTMS on the activity of cortical neurons in an effort to understand the underlying cellular mechanisms activated by rTMS. We used whole-cell patch-clamp recordings in acute rat brain slices and calcium imaging of cultured primary neurons to examine changes in neuronal activity and intracellular calcium respectively. Our results indicate that each TMS pulse caused an immediate and transient activation of voltage gated sodium channels (9.6 ± 1.8 nA at -45 mV, p value < 0.01) in neurons. Short 500 ms 20 Hz rTMS stimulation induced action potentials in a subpopulation of neurons, and significantly increased the steady state current of the neurons at near threshold voltages (at -45 mV: before TMS: I = 130 ± 17 pA, during TMS: I = 215 ± 23 pA, p value = 0.001). rTMS stimulation also led to a delayed increase in intracellular calcium (153.88 ± 61.94% increase from baseline). These results show that rTMS has an immediate and cumulative effect on neuronal activity and intracellular calcium levels, and suggest that rTMS may enhance neuronal responses when combined with an additional motor, sensory or cognitive stimulus. Thus, these results could be translated to optimize rTMS protocols for clinical as well as basic science applications.
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