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Chen Z, Rong L, Xiao L, Rao J, Liu H, Liu T, Chen F, Zhang J, Wang L, Li X, Wei X. Altered amplitude of low-frequency fluctuation and functional connectivity in patients with acute unilateral vestibulopathy: a resting-state fMRI study. Front Neurol 2025; 15:1515262. [PMID: 39871988 PMCID: PMC11769794 DOI: 10.3389/fneur.2024.1515262] [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: 10/22/2024] [Accepted: 12/24/2024] [Indexed: 01/29/2025] Open
Abstract
Objective To investigate changes of brain functional activity in patients with acute unilateral vestibulopathy (AUVP) using functional magnetic resonance imaging (fMRI). Methods We studied 32 AUVP patients and 30 healthy controls (HC) who received resting-state fMRI scanning. Methods of voxel-based amplitude of low-frequency fluctuation (ALFF) and seed-based functional connectivity (FC) were adopted to compare the difference in brain function between the two groups. In addition, we evaluated the associations between abnormal neuroimaging results and clinical data in AUVP patients. Results Compared with HC, patients with AUVP showed lower ALFF in brain regions of bilateral insular, right precentral gyrus, left inferior frontal gyrus and right middle frontal gyrus, as well as higher ALFF in left cerebellar anterior lobe. Using these abnormal brain areas as seeds, we observed decreased FC between left insular and left precuneus in AUVP patients. Furthermore, AUVP patients showed increased FC between left insular and left supplementary motor area. Results of correlation analysis indicated that ALFF value (z-value) in left insular was negatively correlated with the canal paresis value (p = 0.005, r = -0.483), and the FC (z-value) between left insular and left precuneus was negatively correlated with dizziness handicap inventory score (p = 0.012, r = -0.438) in patients with AUVP. Conclusion Patients with AUVP during acute period showed altered functional activity and connectivity in brain regions mainly involved in motor control and vestibular information processing. These changes in brain functional activity and connectivity were potentially attributed to decreased vestibular input resulting from unilateral peripheral vestibular impairment.
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Affiliation(s)
- Zhengwei Chen
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Liangqun Rong
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Lijie Xiao
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Jie Rao
- Department of Neurology, Lishui Central Hospital, Lishui, Zhejiang, China
| | - Haiyan Liu
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Tengfei Liu
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Fei Chen
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Jun Zhang
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Lu Wang
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Xi Li
- Neurology Department, Third Affiliated Hospital of Shanghai University, Wenzhou Third Clinical Institute Affiliated to Wenzhou Medical University, Wenzhou People’s Hospital, Wenzhou, Zhejiang, China
| | - Xiue Wei
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
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Padova D, Ratnanather JT, Faria AV, Agrawal Y. Reduced Vestibular Function is Associated with Cortical Surface Shape Changes in the Frontal Cortex. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2024:2024.11.22.24317807. [PMID: 39606396 PMCID: PMC11601719 DOI: 10.1101/2024.11.22.24317807] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 11/29/2024]
Abstract
Aging-associated decline in peripheral vestibular function is linked to deficits in executive ability, self-motion perception, and motor planning and execution. While these behaviors are known to rely on the sensorimotor and frontal cortices, the precise pathways involving the frontal and sensorimotor cortices in these vestibular-associated behaviors are unknown. To fill this knowledge gap, this cross-sectional study investigates the relationship between age-related variation in vestibular function and surface shape alterations of the frontal and sensorimotor cortices, considering age, intracranial volume, and sex. Data from 117 participants aged 60+ from the Baltimore Longitudinal Study of Aging, who underwent end-organ-specific vestibular tests (cVEMP for the saccule, oVEMP for the utricle, and vHIT for the horizontal canal) and T1-weighted MRI scans on the same visit, were analyzed. We examined ten brain structures in the putative "vestibular cortex": the middle-superior part of the prefrontal cortex (SFG_PFC), frontal pole (SFG_pole), and posterior pars of the superior frontal gyrus (SFG), the dorsal prefrontal cortex and posterior pars of middle frontal gyrus (MFG_DPFC, MFG), the pars opercularis, pars triangularis, and pars orbitalis of the inferior frontal gyrus, as well as the precentral gyrus and postcentral gyrus (PoCG) of the sensori-motor cortex. For each region of interest (ROI), shape descriptors were estimated as local compressions and expansions of the population average ROI surface using surface LDDMM. Shape descriptors were linearly regressed onto standardized vestibular variables, age, intracranial volume, and sex. Lower utricular function was linked with surface compression in the left MFG and expansion in the bilateral SFG_pole and left SFG. Reduced canal function was associated with surface compression in the right SFG_PFC and SFG_pole and left SFG. Both reduced saccular and utricular function correlated with surface compression in the posterior medial part of the left MFG. Our findings illuminate the complexity of the relationship between vestibular function and the morphology of the frontal and sensorimotor cortices in aging. Improved understanding of these relationships could help in developing interventions to enhance quality of life in aging and populations with cognitive impairment.
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Affiliation(s)
- Dominic Padova
- Center for Imaging Science, Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - J. Tilak Ratnanather
- Center for Imaging Science and Institute for Computational Medicine, Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Andreia V. Faria
- Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA
| | - Yuri Agrawal
- Department of Otolaryngology – Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA
- Department of Otolaryngology – Head and Neck Surgery, University of Colorado Anschutz Medical Campus, Aurora, CO, USA
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Chen Z, Cai Y, Liu Y, Liu H, Wei XE, Lin C, Liu D, Xiao L, Rong L. Altered thalamus functional connectivity in patients with acute unilateral vestibulopathy: a resting-state fMRI study. Front Neurosci 2024; 18:1388213. [PMID: 39010942 PMCID: PMC11246849 DOI: 10.3389/fnins.2024.1388213] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/19/2024] [Accepted: 05/31/2024] [Indexed: 07/17/2024] Open
Abstract
Objective Acute unilateral vestibulopathy (AUVP) is the second leading cause of peripheral vestibular vertigo. Full recovery of AUVP is related to sufficient central vestibular compensation. It has been confirmed that the vestibular nucleus and vestibular cortex are involved in the process of vestibular compensatory in AUVP patients. However, few studies have focused on the functional compensation of thalamus in patients with AUVP. This study aimed to explore the alterations of resting-state functional connectivity (FC) focused on thalamus using functional magnetic resonance imaging (fMRI) in AUVP patients. Methods Data of 3D-T1 and resting-state fMRI were collected from 40 AUVP patients and 35 healthy controls (HC). Seeds-based (bilateral thalamus) FC was analyzed to investigate the changes in FC between the two groups. Furthermore, we evaluated the associations between altered thalamus FC and clinical features in AUVP patients using Pearson's partial correlation. Results Compared with HC, AUVP patients showed decreased FC between bilateral thalamus and left insula. We also observed decreased FC between right thalamus and left supramarginal gyrus. Additionally, we found increased FC between left thalamus and right postcentral gyrus (PCG), as well as increased FC between right thalamus and regions of bilateral PCG, right middle frontal gyrus and right middle occipital gyrus in AUVP patients. Furthermore, the FC between left thalamus and left insula was negatively correlated with values of canal paresis in patients with AUVP (p = 0.010, r = -0.434). Conclusion Our results provided first evidence for the decreased thalamo-vestibular cortex pathway, as well as increased thalamo-somatosensory and thalamo-visual cortex pathway in AUVP patients. These findings help us better understand the underlying mechanisms of central dynamic compensatory following an acute unilateral peripheral vestibular damage.
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Affiliation(s)
- Zhengwei Chen
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Yaxian Cai
- Department of Neurology, General Hospital of the Yangtze River Shipping, Wuhan, Hubei, China
| | - Yueji Liu
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Haiyan Liu
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Xiu-e Wei
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Cunxin Lin
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Dan Liu
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Lijie Xiao
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
| | - Liangqun Rong
- Department of Neurology, Second Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu, China
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Schöne CG, Vibert D, Mast FW. Executive functions in patients with bilateral and unilateral peripheral vestibular dysfunction. J Neurol 2024; 271:3291-3308. [PMID: 38466421 PMCID: PMC11136862 DOI: 10.1007/s00415-024-12267-7] [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: 10/31/2023] [Revised: 02/16/2024] [Accepted: 02/17/2024] [Indexed: 03/13/2024]
Abstract
Previous research suggests that patients with peripheral vestibular dysfunction (PVD) suffer from nonspatial cognitive problems, including executive impairments. However, previous studies that assessed executive functions are conflicting, limited to single executive components, and assessments are confounded by other cognitive functions. We compared performance in a comprehensive executive test battery in a large sample of 83 patients with several conditions of PVD (34 bilateral, 29 chronic unilateral, 20 acute unilateral) to healthy controls who were pairwise matched to patients regarding age, sex, and education. We assessed basic and complex executive functions with validated neuropsychological tests. Patients with bilateral PVD performed worse than controls in verbal initiation and working memory span, while other executive functions were preserved. Patients with chronic unilateral PVD had equal executive performance as controls. Patients with acute unilateral PVD performed worse than controls in the exact same tests as patients with bilateral PVD (verbal initiation, working memory span); however, this effect in patients with acute PVD diminished after correcting for multiple comparisons. Hearing loss and affective disorders did not influence our results. Vestibular related variables (disease duration, symptoms, dizziness handicap, deafferentation degree, and compensation) did not predict verbal initiation or working memory span in patients with bilateral PVD. The results suggest that bilateral PVD not only manifests in difficulties when solving spatial tasks but leads to more general neurocognitive deficits. This understanding is important for multidisciplinary workgroups (e.g., neurotologists, neurologists, audiologists) that are involved in diagnosing and treating patients with PVD. We recommend screening patients with PVD for executive impairments and if indicated providing them with cognitive training or psychoeducational support.
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Affiliation(s)
- Corina G Schöne
- Department of Psychology, University of Bern, Bern, Switzerland.
- Department of Otorhinolaryngology, Head and Neck Surgery, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland.
| | - Dominique Vibert
- Department of Otorhinolaryngology, Head and Neck Surgery, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland
| | - Fred W Mast
- Department of Psychology, University of Bern, Bern, Switzerland
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5
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Smith PF. Interpreting the meaning of changes in hippocampal volume associated with vestibular loss. Front Integr Neurosci 2023; 17:1254972. [PMID: 37608860 PMCID: PMC10440551 DOI: 10.3389/fnint.2023.1254972] [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: 07/07/2023] [Accepted: 07/21/2023] [Indexed: 08/24/2023] Open
Abstract
Many studies have documented cognitive deficits, especially spatial cognitive deficits, in patients with some form of vestibular loss. Almost 20 years ago, hippocampal (HPC) atrophy was reported to be correlated with spatial memory deficits in such patients and the idea has gradually emerged that HPC atrophy may be causally responsible for the cognitive deficits. However, the results of studies of HPC volume following vestibular loss have not always been consistent, and a number of studies have reported no evidence of HPC atrophy. This paper argues that HPC atrophy, if it does occur following vestibular loss, may not be directly, causally responsible for the cognitive deficits, and that it is more likely that rapid functional changes in the HPC are responsible, due to the interruption of the transmission of vestibular information to the HPC. The argument presented here rests on 3 tranches of evidence: (1) Cognitive deficits have been observed in humans even in the absence of HPC atrophy; (2) HPC atrophy has not been reported in animal studies following vestibular loss, despite cognitive deficits; and (3) Animal studies have shown that the interruption of the transmission of vestibular information to the HPC has immediate consequences for HPC place cells, far too quickly to be explained by HPC atrophy. It is possible that HPC atrophy, when it does occur, is related to the longer-term consquences of living with vestibular loss, which are likely to increase circulating cortisol.
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Affiliation(s)
- Paul F. Smith
- Department of Pharmacology and Toxicology, Brain Health Research Centre, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand
- The Brain Research New Zealand Centre of Research Excellence, Eisdell Moore Centre for Hearing and Balance Research, University of Auckland, Auckland, New Zealand
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6
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Schöne CG, Rebsamen M, Wyssen G, Rummel C, Wagner F, Vibert D, Mast FW. Hippocampal volume in patients with bilateral and unilateral peripheral vestibular dysfunction. Neuroimage Clin 2022; 36:103212. [PMID: 36209619 PMCID: PMC9668627 DOI: 10.1016/j.nicl.2022.103212] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/22/2022] [Revised: 09/21/2022] [Accepted: 09/28/2022] [Indexed: 12/14/2022]
Abstract
Previous studies have found that peripheral vestibular dysfunction is associated with altered volumes in different brain structures, especially in the hippocampus. However, published evidence is conflicting. Based on previous findings, we compared hippocampal volume, as well as supramarginal, superior temporal, and postcentral gyrus in a sample of 55 patients with different conditions of peripheral vestibular dysfunction (bilateral, chronic unilateral, acute unilateral) to 39 age- and sex-matched healthy controls. In addition, we explored deviations in gray-matter volumes in hippocampal subfields. We also analysed correlations between morphometric data and visuo-spatial performance. Patients with vestibular dysfunction did not differ in total hippocampal volume from healthy controls. However, a reduced volume in the right presubiculum of the hippocampus and the left supramarginal gyrus was observed in patients with chronic and acute unilateral vestibular dysfunction, but not in patients with bilateral vestibular dysfunction. No association of altered volumes with visuo-spatial performance was found. An asymmetric vestibular input due to unilateral vestibular dysfunction might lead to reduced central brain volumes that are involved in vestibular processing.
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Affiliation(s)
- Corina G. Schöne
- Department of Psychology, University of Bern, Bern, Switzerland,Department of Otorhinolaryngology, Head and Neck Surgery, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland,Doctoral Program for Brain and Behavioral Sciences, University of Bern, Bern, Switzerland,Corresponding author.
| | - Michael Rebsamen
- Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland,Graduate School for Cellular and Biomedical Sciences, University of Bern, Bern, Switzerland
| | - Gerda Wyssen
- Department of Psychology, University of Bern, Bern, Switzerland
| | - Christian Rummel
- Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland
| | - Franca Wagner
- Support Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland
| | - Dominique Vibert
- Department of Otorhinolaryngology, Head and Neck Surgery, Inselspital, University Hospital Bern, University of Bern, Bern, Switzerland
| | - Fred W. Mast
- Department of Psychology, University of Bern, Bern, Switzerland
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7
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Si L, Cui B, Li Z, Li X, Li K, Ling X, Shen B, Yang X. Altered Resting-State Intranetwork and Internetwork Functional Connectivity in Patients With Chronic Unilateral Vestibulopathy. J Magn Reson Imaging 2021; 56:291-300. [PMID: 34921750 PMCID: PMC9299943 DOI: 10.1002/jmri.28031] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/22/2021] [Revised: 12/04/2021] [Accepted: 12/08/2021] [Indexed: 11/12/2022] Open
Abstract
BACKGROUND Chronic unilateral vestibulopathy (CUVP) is often accompanied by dizziness and postural instability, which restrict patients' daily activities. It is important to understand central compensation mechanisms underlying these symptoms in patients with CUVP by evaluating their brain functional status. PURPOSE To analyze the changes in resting-state intranetwork and internetwork functional connectivity (FC) and explore the state of central vestibular compensation in patients with CUVP. STUDY TYPE Retrospective. POPULATION Eighteen patients with right-sided CUVP and 18 age- and sex-matched healthy controls. FIELD STRENGTH/SEQUENCE A 3.0 T, three-dimensional magnetization-prepared rapid gradient-echo (MP-RAGE) and resting-state echo-planar imaging (EPI) functional MRI sequences. ASSESSMENT FC alterations were explored using independent component analysis (ICA). Twelve independent components were identified via ICA. Dizziness Handicap Inventory (DHI) score for all patients was determined. STATISTICAL TESTS Two-sample t test, family-wise error (FWE) correction, Pearson correlation coefficient (r). A P value <0.05 was considered statistically significant. RESULTS Compared with healthy controls, patients with CUVP showed significantly decreased FC in the right middle occipital gyrus within the lateral visual network, and significantly increased FC in the right supplementary motor area within the sensorimotor network. The FC was decreased between the medial visual and auditory networks, the right frontoparietal and posterior default networks, as well as the sensorimotor and auditory networks. There was a significant negative correlation between the FC changes in the visual, auditory networks and the DHI score in patients with CUVP (r = -0.583). DATA CONCLUSION Compared to healthy controls, the FC was significantly decreased in the right visual cortex and significantly enhanced in the right sensorimotor network in patients with CUVP. Patients with CUVP showed decreased FC between multiple whole-brain networks, suggesting that abnormal integration of multisensory information may be involved in the occurrence of chronic dizziness and instability in patients with CUVP. LEVEL OF EVIDENCE 4 TECHNICAL EFFICACY: Stage 2.
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Affiliation(s)
- Lihong Si
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Bin Cui
- Department of Radiology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Zheyuan Li
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Xiang Li
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Kangzhi Li
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Xia Ling
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Bo Shen
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
| | - Xu Yang
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, People's Republic of China
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Chronic, Mild Vestibulopathy Leads to Deficits in Spatial Tasks that Rely on Vestibular Input While Leaving Other Cognitive Functions and Brain Volumes Intact. Life (Basel) 2021; 11:life11121369. [PMID: 34947900 PMCID: PMC8707705 DOI: 10.3390/life11121369] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/02/2021] [Revised: 11/30/2021] [Accepted: 12/07/2021] [Indexed: 02/07/2023] Open
Abstract
Objectives: In this study, based on the known vestibulo-hippocampal connections, we asked whether mild chronic vestibulopathy leads only to vestibular-related deficits or whether there are effects on hippocampal function, structure, and cognition in general. In more detail, we assessed whether chronic vestibulopathy leads to (a) deficits in vestibular tasks without cognitive demand (balancing), (b) deficits in spatial cognitive tasks that require vestibular input (path integration, rotational memory), (c) deficits in spatial cognitive tasks that do not rely on vestibular input, (d) deficits in general cognitive function, and (e) atrophy in the brain. Methods: A total of 15 patients with chronic uni- or bilateral vestibulopathy (56.8 ± 10.1 years; 4 females) were included in this study and were age- and gender-matched by the control participants (57.6 ± 10.5) in a pairwise manner. Given their clinical symptoms and their deficits of the vestibulo-ocular reflex (VOR) the patients could be classified as being mildly affected. All participants of the underwent the following tests: clinical balance (CBT), triangle completion (TCT) for path integration, rotational memory (RM), the visuo-spatial subset of the Berlin intelligence structure test (BIS-4) and d2-R for attention and concentration, and a structural MRI for gray matter analysis using voxel-based morphometry (VBM). Results: Compared to the healthy controls, the vestibulopathy patients performed significantly worse in terms of CBT, TCT, and RM but showed no differences in terms of the BIS-4 and d2-R. There were also no significant volumetric gray matter differences between the two groups. Conclusions: This study provides evidence that both non-cognitive and cognitive functions that rely on vestibular input (balancing, path integration, rotational memory) are impaired, even in mild chronic vestibulopathy, while other cognitive functions, which rely on visual input (visuo-spatial memory, attention), are unimpaired in this condition, together with an overall intact brain structure. These findings may reflect a segregation between vestibular- and visual-dependent processes in the medial temporal lobe on the one hand and a structure–function dissociation on the other.
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Lacroix E, Deggouj N, Edwards MG, Van Cutsem J, Van Puyvelde M, Pattyn N. The Cognitive-Vestibular Compensation Hypothesis: How Cognitive Impairments Might Be the Cost of Coping With Compensation. Front Hum Neurosci 2021; 15:732974. [PMID: 34658819 PMCID: PMC8517512 DOI: 10.3389/fnhum.2021.732974] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2021] [Accepted: 09/10/2021] [Indexed: 11/13/2022] Open
Abstract
Previous research in vestibular cognition has clearly demonstrated a link between the vestibular system and several cognitive and emotional functions. However, the most coherent results supporting this link come from rodent models and healthy human participants artificial stimulation models. Human research with vestibular-damaged patients shows much more variability in the observed results, mostly because of the heterogeneity of vestibular loss (VL), and the interindividual differences in the natural vestibular compensation process. The link between the physiological consequences of VL (such as postural difficulties), and specific cognitive or emotional dysfunction is not clear yet. We suggest that a neuropsychological model, based on Kahneman's Capacity Model of Attention, could contribute to the understanding of the vestibular compensation process, and partially explain the variability of results observed in vestibular-damaged patients. Several findings in the literature support the idea of a limited quantity of cognitive resources that can be allocated to cognitive tasks during the compensation stages. This basic mechanism of attentional limitations may lead to different compensation profiles in patients, with or without cognitive dysfunction, depending on the compensation stage. We suggest several objective and subjective measures to evaluate this cognitive-vestibular compensation hypothesis.
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Affiliation(s)
- Emilie Lacroix
- VIPER Research Unit, LIFE Department, Royal Military Academy, Brussels, Belgium.,Institute for Research in Psychological Science (IPSY), Université Catholique de Louvain, Louvain-la-Neuve, Belgium
| | - Naïma Deggouj
- Institute for Research in Psychological Science (IPSY), Université Catholique de Louvain, Louvain-la-Neuve, Belgium.,Institute of Neuroscience (IONS), Université Catholique de Louvain, Louvain-la-Neuve, Belgium.,Otorhinolaryngology Department, Cliniques Universitaires Saint-Luc, Brussels, Belgium
| | - Martin Gareth Edwards
- Institute for Research in Psychological Science (IPSY), Université Catholique de Louvain, Louvain-la-Neuve, Belgium.,Institute of Neuroscience (IONS), Université Catholique de Louvain, Louvain-la-Neuve, Belgium
| | - Jeroen Van Cutsem
- VIPER Research Unit, LIFE Department, Royal Military Academy, Brussels, Belgium.,Human Physiology and Sports Physiotherapy Research Group, Vrije Universiteit Brussel, Brussels, Belgium
| | - Martine Van Puyvelde
- VIPER Research Unit, LIFE Department, Royal Military Academy, Brussels, Belgium.,Brain Body and Cognition Research Group, Department of Psychology and Educational Sciences, Vrije Universiteit Brussel, Brussels, Belgium.,Clinical and Lifespan Psychology, Department of Psychology and Educational Sciences, Vrije Universiteit Brussel, Brussels, Belgium
| | - Nathalie Pattyn
- VIPER Research Unit, LIFE Department, Royal Military Academy, Brussels, Belgium.,Human Physiology and Sports Physiotherapy Research Group, Vrije Universiteit Brussel, Brussels, Belgium
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Er F, Goularas D. Predicting the Prognosis of MCI Patients Using Longitudinal MRI Data. IEEE/ACM TRANSACTIONS ON COMPUTATIONAL BIOLOGY AND BIOINFORMATICS 2021; 18:1164-1173. [PMID: 32813661 DOI: 10.1109/tcbb.2020.3017872] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/11/2023]
Abstract
The aim of this study is to develop a computer-aided diagnosis system with a deep-learning approach for distinguishing "Mild Cognitive Impairment (MCI) due to Alzheimer's Disease (AD)" patients among a list of MCI patients. In this system we are using the power of longitudinal data extracted from magnetic resonance (MR). For this work, a total of 294 MCI patients were selected from the ADNI database. Among them, 125 patients developed AD during their follow-up and the rest remained stable. The proposed computer-aided diagnosis system (CAD) attempts to identify brain regions that are significant for the prediction of developing AD. The longitudinal data were constructed using a 3D Jacobian-based method aiming to track the brain differences between two consecutive follow-ups. The proposed CAD system distinguishes MCI patients who developed AD from those who remained stable with an accuracy of 87.2 percent. Moreover, it does not depend on data acquired by invasive methods or cognitive tests. This work demonstrates that the use of data in different time periods contains information that is beneficial for prognosis prediction purposes that outperform similar methods and are slightly inferior only to those systems that use invasive methods or neuropsychological tests.
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11
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Li K, Si L, Cui B, Ling X, Shen B, Yang X. Altered spontaneous functional activity of the right precuneus and cuneus in patients with persistent postural-perceptual dizziness. Brain Imaging Behav 2021; 14:2176-2186. [PMID: 31313022 DOI: 10.1007/s11682-019-00168-7] [Citation(s) in RCA: 19] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/24/2022]
Abstract
Persistent postural-perceptual dizziness (PPPD) is a functional vestibular disorder, and is the most common cause of chronic vestibular syndrome. However, the pathogenesis of PPPD is currently unclear. This study aimed to analyze the changes of brain spontaneous functional activities in PPPD patients during the resting state, and to explore the underlying pathogenesis of PPPD, particularly the abnormal integration of visual and vestibular information. Ten PPPD patients and 10 healthy controls were enrolled from January to June 2018, and baseline data were collected from all subjects. Videonystagmography (VNG), the vestibular caloric test, the video head impulse test (vHIT) and vestibular evoked myogenic potentials (VEMPs) were measured to exclude peripheral vestibular lesions. Functional MRI (fMRI) was conducted in PPPD patients and healthy controls. The amplitude of low frequency fluctuation (ALFF) and regional homogeneity (ReHo), and functional connectivity were calculated to explore changes in brain spontaneous functional activity during the resting state. Compared with healthy controls, ALFF and ReHo values in the right precuneus and cuneus were significantly lower in PPPD patients (both P < 0.05). Further seed-based functional connectivity analysis showed decreased functional connectivity between precuneus, cuneus and left precentral gyrus (P < 0.05). Our findings suggest that the spontaneous functional activity of cuneus and precuneus in PPPD patients were altered, potentially leading to abnormal integration of visual and vestibular information. Weakened functional connectivity between the precuneus and the precentral gyrus may be associated with aggravated symptoms during upright posture, active or passive movements.
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Affiliation(s)
- Kangzhi Li
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, 100049, People's Republic of China
| | - Lihong Si
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, 100049, People's Republic of China
| | - Bin Cui
- Department of Radiology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, 100049, People's Republic of China
| | - Xia Ling
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, 100049, People's Republic of China
| | - Bo Shen
- Department of Neurology, The First Affiliated Hospital of Jinzhou Medical University, Jinzhou, 121001, People's Republic of China
| | - Xu Yang
- Department of Neurology, Aerospace Center Hospital, Peking University Aerospace School of Clinical Medicine, Beijing, 100049, People's Republic of China.
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12
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Zhang YN, Li H, Shen ZW, Xu C, Huang YJ, Wu RH. Healthy individuals vs patients with bipolar or unipolar depression in gray matter volume. World J Clin Cases 2021; 9:1304-1317. [PMID: 33644197 PMCID: PMC7896697 DOI: 10.12998/wjcc.v9.i6.1304] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/10/2020] [Revised: 12/14/2020] [Accepted: 12/23/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Previous studies using voxel-based morphometry (VBM) revealed changes in gray matter volume (GMV) of patients with depression, but the differences between patients with bipolar disorder (BD) and unipolar depression (UD) are less known.
AIM To analyze the whole-brain GMV data of patients with untreated UD and BD compared with healthy controls.
METHODS Fourteen patients with BD and 20 with UD were recruited from the Mental Health Center of Shantou University between August 2014 and July 2015, and 20 non-depressive controls were recruited. After routine three-plane positioning, axial T2WI scanning was performed. The connecting line between the anterior and posterior commissures was used as the scanning baseline. The scanning range extended from the cranial apex to the foramen magnum. Categorical data are presented as frequencies and were analyzed using the Fisher exact test.
RESULTS There were no significant intergroup differences in gender, age, or years of education. Disease course, age at the first episode, and Hamilton depression rating scale scores were similar between patients with UD and those with BD. Compared with the non-depressive controls, patients with BD showed smaller GMVs in the right inferior temporal gyrus, left middle temporal gyrus, right middle occipital gyrus, and right superior parietal gyrus and larger GMVs in the midbrain, left superior frontal gyrus, and right cerebellum. In contrast, UD patients showed smaller GMVs than the controls in the right fusiform gyrus, left inferior occipital gyrus, left paracentral lobule, right superior and inferior temporal gyri, and the right posterior lobe of the cerebellum, and larger GMVs than the controls in the left posterior central gyrus and left middle frontal gyrus. There was no difference in GMV between patients with BD and UD.
CONCLUSION Using VBM, the present study revealed that patients with UD and BD have different patterns of changes in GMV when compared with healthy controls.
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Affiliation(s)
- Yin-Nan Zhang
- Department of Rehabilitation Medicine, Mental Health Center of Shantou University, Shantou 515000, Guangdong Province, China
| | - Hui Li
- Mental Health Center of Shantou University, Shantou 515000, Guangdong Province, China
| | | | - Chang Xu
- Mental Health Center of Shantou University, Shantou 515000, Guangdong Province, China
| | - Yue-Jun Huang
- Department of Pediatrics, The Second Affiliated Hospital of Shantou University Medical College, Shantou 515000, Guangdong Province, China
| | - Ren-Hua Wu
- Department of Medical Imaging, The Second Affiliated Hospital of Shantou University Medical College, Shantou 515041, Guangdong Province, China
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13
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Conrad J, Habs M, Boegle R, Ertl M, Kirsch V, Stefanova-Brostek I, Eren O, Becker-Bense S, Stephan T, Wollenweber F, Duering M, Zu Eulenburg P, Dieterich M. Global multisensory reorganization after vestibular brain stem stroke. Ann Clin Transl Neurol 2020; 7:1788-1801. [PMID: 32856758 PMCID: PMC7545594 DOI: 10.1002/acn3.51161] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/13/2020] [Accepted: 07/25/2020] [Indexed: 12/14/2022] Open
Abstract
OBJECTIVE Patients with acute central vestibular syndrome suffer from vertigo, spontaneous nystagmus, postural instability with lateral falls, and tilts of visual vertical. Usually, these symptoms compensate within months. The mechanisms of compensation in vestibular infarcts are yet unclear. This study focused on structural changes in gray and white matter volume that accompany clinical compensation. METHODS We studied patients with acute unilateral brain stem infarcts prospectively over 6 months. Structural changes were compared between the acute phase and follow-up with a group of healthy controls using voxel-based morphometry. RESULTS Restitution of vestibular function following brain stem infarcts was accompanied by downstream structural changes in multisensory cortical areas. The changes depended on the location of the infarct along the vestibular pathways in patients with pathological tilts of the SVV and on the quality of the vestibular percept (rotatory vs graviceptive) in patients with pontomedullary infarcts. Patients with pontomedullary infarcts with vertigo or spontaneous nystagmus showed volumetric increases in vestibular parietal opercular multisensory and (retro-) insular areas with right-sided preference. Compensation of graviceptive deficits was accompanied by adaptive changes in multiple multisensory vestibular areas in both hemispheres in lower brain stem infarcts and by additional changes in the motor system in upper brain stem infarcts. INTERPRETATION This study demonstrates multisensory neuroplasticity in both hemispheres along with the clinical compensation of vestibular deficits following unilateral brain stem infarcts. The data further solidify the concept of a right-hemispheric specialization for core vestibular processing. The identification of cortical structures involved in central compensation could serve as a platform to launch novel rehabilitative treatments such as transcranial stimulations.
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Affiliation(s)
- Julian Conrad
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany
| | - Maximilian Habs
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany
| | - Rainer Boegle
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,Graduate School of Systemic Neurosciences - GSN-LMU, LMU Munich, Munich, Germany
| | - Matthias Ertl
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,Department of Psychology, University of Bern, Bern, Switzerland
| | - Valerie Kirsch
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany.,Graduate School of Systemic Neurosciences - GSN-LMU, LMU Munich, Munich, Germany
| | | | - Ozan Eren
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany
| | - Sandra Becker-Bense
- German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany
| | - Thomas Stephan
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany
| | - Frank Wollenweber
- Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany.,Department of Neurology, Helios Dr. Horst Schmidt Kliniken, Wiesbaden, Germany
| | - Marco Duering
- Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany.,Munich Cluster for Systems Neurology (SyNergy), Munich, Germany
| | - Peter Zu Eulenburg
- German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany.,Graduate School of Systemic Neurosciences - GSN-LMU, LMU Munich, Munich, Germany.,Institute for Neuroradiology, University Hospital, LMU Munich, Munich, Germany
| | - Marianne Dieterich
- Department of Neurology, University Hospital, LMU Munich, Munich, Germany.,German Center for Vertigo and Balance Disorders (DSGZ), University Hospital, LMU Munich, Munich, Germany.,Graduate School of Systemic Neurosciences - GSN-LMU, LMU Munich, Munich, Germany.,Munich Cluster for Systems Neurology (SyNergy), Munich, Germany
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14
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Liu L, Hu X, Zhang Y, Pan Q, Zhan Q, Tan G, Wang K, Zhou J. Effect of Vestibular Rehabilitation on Spontaneous Brain Activity in Patients With Vestibular Migraine: A Resting-State Functional Magnetic Resonance Imaging Study. Front Hum Neurosci 2020; 14:227. [PMID: 32595463 PMCID: PMC7303278 DOI: 10.3389/fnhum.2020.00227] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/16/2019] [Accepted: 05/20/2020] [Indexed: 12/20/2022] Open
Abstract
Previous studies have shown that vestibular migraine (VM) is a cerebral disease with recurrent vertigo. Vestibular rehabilitation (VR) is an effective type of physical therapy for minimizing vestibular symptoms, as it improves vestibular compensation in patients with VM. Currently, the cerebral regions that are associated with the pathogenesis of VM are largely unknown. To further understand the underlying mechanisms of VM, we performed resting-state functional magnetic resonance imaging (fMRI) before and after 1 month of VR in 14 patients with VM. The Dizziness Handicap Inventory (DHI), the 36-Item Short-Form Health Survey (SF-36), the Hamilton Depression Scale (HAMD) and the Hamilton Anxiety Scale (HAMA) scores were included as clinical outcomes. The amplitude of low-frequency fluctuation (ALFF) was assessed to characterize spontaneous brain activity. The correlations between the clinical characteristics and ALFF values were assessed. After 1 month of VR training, the DHI scores in patients with VM were significantly lower than those at baseline (p = 0.03), as were the HAMA scores (p = 0.02). We also found that the ALFF values in the left posterior cerebellum of VM patients increased significantly after 1 month of VR training. Moreover, the ALFF values in the left cerebellum were inversely correlated with the patients’ DHI scores. Overall, this study showed that VR exercise for 1 month has a positive effect on vestibular symptoms in patients with VM. Asymmetric cerebellar hyperactivity might be a functional compensation for vestibular dysfunction in patients with VM.
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Affiliation(s)
- Li Liu
- Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China.,Department of Neurology, Chongqing Renji Hospital, University of Chinese Academy of Sciences, Chongqing, China
| | - Xiaofei Hu
- Department of Radiology, Southwest Hospital, Third Military Medical University (Army Medical University), Chongqing, China
| | - Yixin Zhang
- Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
| | - Qi Pan
- Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
| | - Qunling Zhan
- Department of Neurology, Chongqing Renji Hospital, University of Chinese Academy of Sciences, Chongqing, China
| | - Ge Tan
- Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
| | - Kuiyun Wang
- Department of Neurology, The Jintang First People's Hospital, Sichuan University, Sichuan, China
| | - Jiying Zhou
- Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China
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15
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Which Effects on Neuroanatomy and Path-Integration Survive? Results of a Randomized Controlled Study on Intensive Balance Training. Brain Sci 2020; 10:brainsci10040210. [PMID: 32260099 PMCID: PMC7226327 DOI: 10.3390/brainsci10040210] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/06/2020] [Revised: 03/27/2020] [Accepted: 03/31/2020] [Indexed: 12/12/2022] Open
Abstract
Balancing is a complex task requiring the integration of visual, somatosensory and vestibular inputs. The vestibular system is linked to the hippocampus, a brain structure crucial for spatial orientation. Here we tested the immediate and sustained effects of a one-month-long slackline training program on balancing and orientation abilities as well as on brain volumes in young adults without any prior experience in that skill. On the corrected level, we could not find any interaction effects for brain volumes, but the effect sizes were small to medium. A subsequent within-training-group analysis revealed volumetric increments within the somatosensory cortex and decrements within posterior insula, cerebellum and putamen remained stable over time. No significant interaction effects were observed on the clinical balance and the spatial orientation task two months after the training period (follow-up). We interpret these findings as a shift away from processes crucial for automatized motor output towards processes related to voluntarily controlled movements. The decrease in insular volume in the training group we propose to result from multisensory interaction of the vestibular with the visual and somatosensory systems. The discrepancy between sustained effects in the brain of the training group on the one hand and transient benefits in function on the other may indicate that for the latter to be retained a longer-term practice is required.
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16
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Park JH, Jeon HJ, Lim EC, Koo JW, Lee HJ, Kim HJ, Lee JS, Song CG, Hong SK. Feasibility of Eye Tracking Assisted Vestibular Rehabilitation Strategy Using Immersive Virtual Reality. Clin Exp Otorhinolaryngol 2019; 12:376-384. [PMID: 31066247 PMCID: PMC6787482 DOI: 10.21053/ceo.2018.01592] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/02/2018] [Accepted: 03/14/2019] [Indexed: 11/22/2022] Open
Abstract
OBJECTIVES Even though vestibular rehabilitation therapy (VRT) using head-mounted display (HMD) has been highlighted recently as a popular virtual reality platform, we should consider that HMD itself do not provide interactive environment for VRT. This study aimed to test the feasibility of interactive components using eye tracking assisted strategy through neurophysiologic evidence. METHODS HMD implemented with an infrared-based eye tracker was used to generate a virtual environment for VRT. Eighteen healthy subjects participated in our experiment, wherein they performed a saccadic eye exercise (SEE) under two conditions of feedback-on (F-on, visualization of eye position) and feedback-off (F-off, non-visualization of eye position). Eye position was continuously monitored in real time on those two conditions, but this information was not provided to the participants. Electroencephalogram recordings were used to estimate neural dynamics and attention during SEE, in which only valid trials (correct responses) were included in electroencephalogram analysis. RESULTS SEE accuracy was higher in the F-on than F-off condition (P=0.039). The power spectral density of beta band was higher in the F-on condition on the frontal (P=0.047), central (P=0.042), and occipital areas (P=0.045). Beta-event-related desynchronization was significantly more pronounced in the F-on (-0.19 on frontal and -0.22 on central clusters) than in the F-off condition (0.23 on frontal and 0.05 on central) on preparatory phase (P=0.005 for frontal and P=0.024 for central). In addition, more abundant functional connectivity was revealed under the F-on condition. CONCLUSION Considering substantial gain may come from goal directed attention and activation of brain-network while performing VRT, our preclinical study from SEE suggests that eye tracking algorithms may work efficiently in vestibular rehabilitation using HMD.
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Affiliation(s)
- Jeong Hye Park
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea.,Laboratory of Brain and Cognitive Sciences for Convergence Medicine, Hallym University College of Medicine, Anyang, Korea
| | - Han Jae Jeon
- Department of Convergence Software, Hallym University, Chuncheon, Korea
| | - Eun-Cheon Lim
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea.,Laboratory of Brain and Cognitive Sciences for Convergence Medicine, Hallym University College of Medicine, Anyang, Korea
| | - Ja-Won Koo
- Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Bundang Hospital, Seongnam, Korea
| | - Hyo-Jeong Lee
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea.,Laboratory of Brain and Cognitive Sciences for Convergence Medicine, Hallym University College of Medicine, Anyang, Korea
| | - Hyung-Jong Kim
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea
| | - Jung Seop Lee
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea
| | - Chang-Geun Song
- Department of Convergence Software, Hallym University, Chuncheon, Korea
| | - Sung Kwang Hong
- Department of Otorhinolaryngology-Head and Neck Surgery, Hallym University College of Medicine, Anyang, Korea.,Laboratory of Brain and Cognitive Sciences for Convergence Medicine, Hallym University College of Medicine, Anyang, Korea
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17
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Micarelli A, Viziano A, Panella M, Micarelli E, Alessandrini M. Power spectra prognostic aspects of impulsive eye movement traces in superior vestibular neuritis. Med Biol Eng Comput 2019; 57:1617-1627. [DOI: 10.1007/s11517-019-01982-3] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/10/2018] [Accepted: 04/08/2019] [Indexed: 12/01/2022]
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18
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Cerebral perfusion abnormalities in patients with persistent postural-perceptual dizziness (PPPD): a SPECT study. J Neural Transm (Vienna) 2018; 126:123-129. [PMID: 30382406 DOI: 10.1007/s00702-018-1948-3] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/06/2018] [Accepted: 10/23/2018] [Indexed: 10/28/2022]
Abstract
Persistent postural-perceptual dizziness (PPPD) is a recently defined syndrome with chronic dizziness interrupting daily life. Although the high levels of anxiety and functional changes in postural control strategy and multi-sensory information processing and integration may be underlying the pathophysiology, its neural mechanisms are poorly understood. The aim of this study was to examine the regional cerebral blood flow (rCBF) in patients with PPPD using single photon emission computed tomography (SPECT). A total of 25 patients with PPPD and 25 healthy controls participated in the study. All participants underwent brain SPECT and the patients completed the Dizziness Handicap Inventory. SPECT images were compared between the groups, and the correlation of rCBF and disease severity/duration was assessed in patients. Compared with controls, PPPD patients showed a significantly decreased rCBF in the insula and frontal lobe, mainly in the left posterior insula, bilateral superior frontal gyrus, right inferior frontal gyrus, right precentral gyrus, and left medial orbital gyrus. Additionally, PPPD patients showed a significant rCBF increase in the bilateral cerebellum compared with controls. The results of our study suggest that the altered rCBF in the insular, frontal, and cerebellar cortices might be reflecting the process of maladaptation and the compensatory responses for the changes in PPPD.
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19
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An fMRI study of visuo-vestibular interactions following vestibular neuritis. NEUROIMAGE-CLINICAL 2018; 20:1010-1017. [PMID: 30336357 PMCID: PMC6197146 DOI: 10.1016/j.nicl.2018.10.007] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 02/21/2018] [Revised: 10/01/2018] [Accepted: 10/08/2018] [Indexed: 11/22/2022]
Abstract
Vestibular neuritis (VN) is characterised by acute vertigo due to a sudden loss of unilateral vestibular function. A considerable proportion of VN patients proceed to develop chronic symptoms of dizziness, including visually induced dizziness, specifically during head turns. Here we investigated whether the development of such poor clinical outcomes following VN, is associated with abnormal visuo-vestibular cortical processing. Accordingly, we applied functional magnetic resonance imaging to assess brain responses of chronic VN patients and compared these to controls during both congruent (co-directional) and incongruent (opposite directions) visuo-vestibular stimulation (i.e. emulating situations that provoke symptoms in patients). We observed a focal significant difference in BOLD signal in the primary visual cortex V1 between patients and controls in the congruent condition (small volume corrected level of p < .05 FWE). Importantly, this reduced BOLD signal in V1 was negatively correlated with functional status measured with validated clinical questionnaires. Our findings suggest that central compensation and in turn clinical outcomes in VN are partly mediated by adaptive mechanisms associated with the early visual cortex.
VN clinical status related to V1 response to congruent visuo-vestibular stimuli Reduced V1 BOLD signal during congruent stimulation correlates with subjective dizziness scores No association between V1 BOLD signal and incongruent visuo-vestibular stimulation Changes in V1 activity may reflect cortical adaptive mechanisms following VN
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20
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Rusanescu G, Mao J. Peripheral nerve injury induces adult brain neurogenesis and remodelling. J Cell Mol Med 2016; 21:299-314. [PMID: 27665307 PMCID: PMC5264155 DOI: 10.1111/jcmm.12965] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2016] [Accepted: 08/01/2016] [Indexed: 02/06/2023] Open
Abstract
Unilateral peripheral nerve chronic constriction injury (CCI) has been widely used as a research model of human neuropathic pain. Recently, CCI has been shown to induce spinal cord adult neurogenesis, which may contribute to the chronic increase in nociceptive sensitivity. Here, we show that CCI also induces rapid and profound asymmetrical anatomical rearrangements in the adult rodent cerebellum and pons. This remodelling occurs throughout the hindbrain, and in addition to regions involved in pain processing, also affects other sensory modalities. We demonstrate that these anatomical changes, partially reversible in the long term, result from adult neurogenesis. Neurogenic markers Mash1, Ngn2, doublecortin and Notch3 are widely expressed in the rodent cerebellum and pons, both under normal and injured conditions. CCI-induced hindbrain structural plasticity is absent in Notch3 knockout mice, a strain with impaired neuronal differentiation, demonstrating its dependence on adult neurogenesis. Grey matter and white matter structural changes in human brain, as a result of pain, injury or learned behaviours have been previously detected using non-invasive neuroimaging techniques. Because neurogenesis-mediated structural plasticity is thought to be restricted to the hippocampus and the subventricular zone, such anatomical rearrangements in other parts of the brain have been thought to result from neuronal plasticity or glial hypertrophy. Our findings suggest the presence of extensive neurogenesis-based structural plasticity in the adult mammalian brain, which may maintain a memory of basal sensory levels, and act as an adaptive mechanism to changes in sensory inputs.
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Affiliation(s)
- Gabriel Rusanescu
- MGH Center for Translational Pain Research, Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
| | - Jianren Mao
- MGH Center for Translational Pain Research, Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
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21
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Micarelli A, Chiaravalloti A, Schillaci O, Ottaviani F, Alessandrini M. Aspects of cerebral plasticity related to clinical features in acute vestibular neuritis: a "starting point" review from neuroimaging studies. ACTA OTORHINOLARYNGOLOGICA ITALICA 2016; 36:75-84. [PMID: 27196070 PMCID: PMC4907164 DOI: 10.14639/0392-100x-642] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 03/14/2015] [Accepted: 07/25/2015] [Indexed: 11/23/2022]
Abstract
Vestibular neuritis (VN) is one of the most common causes of vertigo and is characterised by a sudden unilateral vestibular failure (UVF). Many neuroimaging studies in the last 10 years have focused on brain changes related to sudden vestibular deafferentation as in VN. However, most of these studies, also due to different possibilities across diverse centres, were based on different times of first acquisition from the onset of VN symptoms, neuroimaging techniques, statistical analysis and correlation with otoneurological and psychological findings. In the present review, the authors aim to merge together the similarities and discrepancies across various investigations that have employed neuroimaging techniques and group analysis with the purpose of better understanding about how the brain changes and what characteristic clinical features may relate to each other in the acute phase of VN. Six studies that strictly met inclusion criteria were analysed to assess cortical-subcortical correlates of acute clinical features related to VN. The present review clearly reveals that sudden UVF may induce a wide variety of cortical and subcortical responses - with changes in different sensory modules - as a result of acute plasticity in the central nervous system.
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Affiliation(s)
- A Micarelli
- Ear-Nose-Throat Unit, "Tor Vergata" University, Rome, Italy;,Systems Medicine Department, Neuroscience Unit, "Tor Vergata" University, Rome, Italy
| | - A Chiaravalloti
- Department of Biomedicine and Prevention, "Tor Vergata" University, Rome, Italy
| | - O Schillaci
- Department of Biomedicine and Prevention, "Tor Vergata" University, Rome, Italy;,IRCCS Neuromed, Pozzilli, Italy
| | - F Ottaviani
- Ear-Nose-Throat Unit, "Tor Vergata" University, Rome, Italy
| | - M Alessandrini
- Ear-Nose-Throat Unit, "Tor Vergata" University, Rome, Italy
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22
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Lacour M, Helmchen C, Vidal PP. Vestibular compensation: the neuro-otologist's best friend. J Neurol 2016; 263 Suppl 1:S54-64. [PMID: 27083885 PMCID: PMC4833803 DOI: 10.1007/s00415-015-7903-4] [Citation(s) in RCA: 180] [Impact Index Per Article: 20.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/03/2015] [Revised: 09/09/2015] [Accepted: 09/10/2015] [Indexed: 02/05/2023]
Abstract
Why vestibular compensation (VC) after an acute unilateral vestibular loss is the neuro-otologist’s best friend is the question at the heart of this paper. The different plasticity mechanisms underlying VC are first reviewed, and the authors present thereafter the dual concept of vestibulo-centric versus distributed learning processes to explain the compensation of deficits resulting from the static versus dynamic vestibular imbalance. The main challenges for the plastic events occurring in the vestibular nuclei (VN) during a post-lesion critical period are neural protection, structural reorganization and rebalance of VN activity on both sides. Data from animal models show that modulation of the ipsilesional VN activity by the contralateral drive substitutes for the normal push–pull mechanism. On the other hand, sensory and behavioural substitutions are the main mechanisms implicated in the recovery of the dynamic functions. These newly elaborated sensorimotor reorganizations are vicarious idiosyncratic strategies implicating the VN and multisensory brain regions. Imaging studies in unilateral vestibular loss patients show the implication of a large neuronal network (VN, commissural pathways, vestibulo-cerebellum, thalamus, temporoparietal cortex, hippocampus, somatosensory and visual cortical areas). Changes in gray matter volume in these multisensory brain regions are structural changes supporting the sensory substitution mechanisms of VC. Finally, the authors summarize the two ways to improve VC in humans (neuropharmacology and vestibular rehabilitation therapy), and they conclude that VC would follow a “top-down” strategy in patients with acute vestibular lesions. Future challenges to understand VC are proposed.
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Affiliation(s)
- Michel Lacour
- Université Aix-Marseille/CNRS, UMR 7260, Fédération de Recherche 3C, Centre de St Charles, 3 Place Victor Hugo, 13331, Marseille Cedex 03, France. .,, 21 Impasse des Vertus, 13710, Fuveau, France.
| | - Christoph Helmchen
- Department of Neurology, University Hospitals Schleswig-Holstein, University of Lübeck, Ratzeburger Allee 160, 23538, Lübeck, Germany
| | - Pierre-Paul Vidal
- Université Paris Descartes/CNRS, UMR-MD-SSA, COGNAC-G (COGNition and Action Group), 45 Rue des Saints Pères, 75270, Paris Cedex 06, France
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Göttlich M, Jandl NM, Sprenger A, Wojak JF, Münte TF, Krämer UM, Helmchen C. Hippocampal gray matter volume in bilateral vestibular failure. Hum Brain Mapp 2016; 37:1998-2006. [PMID: 26918638 DOI: 10.1002/hbm.23152] [Citation(s) in RCA: 51] [Impact Index Per Article: 5.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/14/2015] [Accepted: 02/11/2016] [Indexed: 01/26/2023] Open
Abstract
Bilateral vestibular failure (BVF) is a severe chronic disorder of the labyrinth or the eighth cranial nerve characterized by unsteadiness of gait and disabling oscillopsia during head movements. According to animal data, vestibular input to the hippocampus is proposed to contribute to spatial memory and spatial navigation. Except for one seminal study showing the association of impaired spatial navigation and hippocampal atrophy, patient data in BVF are lacking. Therefore, we performed a voxel-wise comparison of the hippocampal gray matter volume (GMV) in a clinically representative sample of 27 patients with incomplete BVF and 29 age- and gender-matched healthy controls to test the hypothesis of hippocampal atrophy in BVF. Although the two groups did not generally differ in their hippocampal GMV, a reduction of GMV in the bilateral hippocampal CA3 region was significantly correlated with increased vestibulopathy-related clinical impairment. We propose that GMV reduction in the hippocampus of BVF patients is related to the severity of vestibular-induced disability which is in line with combined hippocampal atrophy and disorders of spatial navigation in complete vestibular deafferentation due to bilateral nerve section. Clinically, however, the most frequent etiologies of BVF cause incomplete lesions. Accordingly, hippocampus atrophy and deficits in spatial navigation occur possibly less frequently than previously suspected. Hum Brain Mapp 37:1998-2006, 2016. © 2016 Wiley Periodicals, Inc.
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Affiliation(s)
- Martin Göttlich
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany
| | - Nico M Jandl
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany
| | - Andreas Sprenger
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany.,Institute of Psychology II, University of Lübeck, Lübeck, Germany
| | - Jann F Wojak
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany
| | - Thomas F Münte
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany.,Institute of Psychology II, University of Lübeck, Lübeck, Germany
| | - Ulrike M Krämer
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany.,Institute of Psychology II, University of Lübeck, Lübeck, Germany
| | - Christoph Helmchen
- Department of Neurology, University of Lübeck and University Hospital Schleswig-Holstein, Lübeck, Germany
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