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Zaffanello M, Pietrobelli A, Nosetti L, Ferrante G, Rigotti E, Ganzarolli S, Piacentini G. Sleep-Disordered Breathing and Central Respiratory Control in Children: A Comprehensive Review. CHILDREN (BASEL, SWITZERLAND) 2025; 12:279. [PMID: 40150562 PMCID: PMC11940935 DOI: 10.3390/children12030279] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/10/2025] [Revised: 02/21/2025] [Accepted: 02/21/2025] [Indexed: 03/29/2025]
Abstract
Background/Objectives: Sleep-disordered breathing (SDB) is a primary concern in children's health. Research suggests that repeated oxygen drops during sleep-common in SDB-may harm the brainstem's breathing control centres. This damage likely occurs through oxidative stress, inflammation, and cell death, which weaken the brain's ability to regulate breathing. Over time, these effects could lead to functional changes (e.g., disrupted chemical signalling) and physical damage in critical brain regions, creating a cycle of unstable breathing. However, much of this evidence comes from animal or lab studies, leaving gaps in our understanding of how these mechanisms work in humans. This review synthesises existing research on how breathing disruptions during sleep-particularly episodes of intermittent hypoxia-affect the brain's ability to control respiration in children and adolescents. Methods: We analysed studies from medical databases PubMed, Scopus, and Web of Science, focusing on how SDB (obstructive or central sleep apnoea) impacts the brain's respiratory centres in young populations. Animal studies and research involving children on mechanical ventilation were excluded to focus on natural sleep patterns. Results: After removing duplicates, 54 studies remained. Additionally, 43 record were excluded for various reasons. Ultimately, 11 articles were selected for the final analysis, including three that focused on genetic conditions, such as Down syndrome, Prader-Willi syndrome, and Pierre Robin sequence. The findings suggest that repeated oxygen dips during sleep may harm the brainstem's respiratory control areas, especially during critical developmental stages. This damage could lead to long-term issues, such as unstable breathing, cardiovascular strain, or neurological problems. However, most studies only captured the immediate effects of low oxygen, leaving uncertainty about permanent harm due to a lack of long-term follow-up. Conclusions: Repeated oxygen deprivation during sleep appears to damage the brainstem and disrupt breathing regulation. However, small study sizes and short observation periods limit the strength of these conclusions. Future research should use advanced imaging tools to clarify long-term risks, develop effective treatments, and track children over extended periods. More significantly, longer-term studies are urgently needed to guide clinical care for vulnerable populations.
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Affiliation(s)
- Marco Zaffanello
- Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, 37126 Verona, Italy; (A.P.); (G.F.); (E.R.); (G.P.)
| | - Angelo Pietrobelli
- Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, 37126 Verona, Italy; (A.P.); (G.F.); (E.R.); (G.P.)
| | - Luana Nosetti
- Lombardy Regional SIDS Center, Division of Pediatrics, F. Del Ponte Hospital, University of Insubria, 21100 Varese, Italy;
| | - Giuliana Ferrante
- Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, 37126 Verona, Italy; (A.P.); (G.F.); (E.R.); (G.P.)
| | - Erika Rigotti
- Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, 37126 Verona, Italy; (A.P.); (G.F.); (E.R.); (G.P.)
| | - Stefania Ganzarolli
- Pediatric Division, Azienda Ospedaliera Universitaria Integrata, 37126 Verona, Italy;
| | - Giorgio Piacentini
- Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, 37126 Verona, Italy; (A.P.); (G.F.); (E.R.); (G.P.)
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Burstein O, Sabag M, Kurtzman L, Geva R. The role of focused attention in learning from early childhood to late adolescence: Implications of neonatal brainstem compromise following preterm birth. Child Dev 2025; 96:269-285. [PMID: 39297250 DOI: 10.1111/cdev.14167] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/03/2025]
Abstract
This comprehensive longitudinal study explored for the first time the interrelations between neonatal brainstem abnormalities, focused attention (FA), and learning-following a preterm cohort (N = 175; 46.3% female; predominantly White) from birth (2003-2006) to 17 years. The findings indicated that FA during early childhood was associated with language outcomes in toddlerhood (n = 131) and academic and attention self-report indices in late adolescence (n = 44). Pilot assessments indicated that FA at 17 years (n = 25) was also associated with concurrent academic and attention functioning. Structural equation modeling analyses revealed that neonatal brainstem functioning, manifested in auditory brainstem response patterns, was associated with early-life FA competence, which affected learning development. Implications underscore the essential role of early brainstem function and FA in shaping childhood learning trajectories.
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Affiliation(s)
- Or Burstein
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel
| | - Maya Sabag
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel
- The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel
| | - Lea Kurtzman
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel
| | - Ronny Geva
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel
- The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel
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3
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Wass SV, Mirza FU, Smith C. Understanding allostasis: Early-life self-regulation involves both up- and down-regulation of arousal. Child Dev 2024; 95:2000-2014. [PMID: 39056636 PMCID: PMC11579635 DOI: 10.1111/cdev.14136] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 07/28/2024]
Abstract
Optimal performance lies at intermediate autonomic arousal, but no previous research has examined whether the emergence of endogenous control associates with changes in children's up-regulation from hypo-arousal, as well as down-regulation from hyper-arousal. We used wearables to take day-long recordings from N = 58, 12-month-olds (60% white/58% female); and, in the same infants, we measured self-regulation in the lab with a still-face paradigm. Overall, our findings suggest that infants who showed more self-regulatory behaviors in the lab were more likely to actively change their behaviors in home settings moment-by-moment "on the fly" following changes in autonomic arousal, and that these changes result in up- as well as down-regulation. Implications for the role of atypical self-regulation in later psychopathology are discussed.
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Affiliation(s)
- S. V. Wass
- Department of PsychologyUniversity of East LondonLondonUK
| | - F. U. Mirza
- Department of PsychologyUniversity of East LondonLondonUK
| | - C. Smith
- Institute of Psychiatry, Psychology & NeuroscienceKing's College LondonLondonUK
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Wingfield KK, Misic T, Jain K, McDermott CS, Abney NM, Richardson KT, Rubman MB, Beierle JA, Miracle SA, Sandago EJ, Baskin BM, Lynch WB, Borrelli KN, Yao EJ, Wachman EM, Bryant CD. The ultrasonic vocalization (USV) syllable profile during neonatal opioid withdrawal and a kappa opioid receptor component to increased USV emissions in female mice. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.07.02.601766. [PMID: 39005445 PMCID: PMC11244951 DOI: 10.1101/2024.07.02.601766] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 07/16/2024]
Abstract
Rationale Opioid use during pregnancy can lead to negative infant health outcomes, including neonatal opioid withdrawal syndrome (NOWS). NOWS comprises gastrointestinal, autonomic nervous system, and neurological dysfunction that manifest during spontaneous withdrawal. Variability in NOWS severity necessitates a more individualized treatment approach. Ultrasonic vocalizations (USVs) in neonatal mice are emitted in isolation as a stress response and are increased during opioid withdrawal, thus modeling a negative affective state that can be utilized to test new treatments. Objectives We sought to identify the behavioral and USV profile, brainstem transcriptomic adaptations, and role of kappa opioid receptors in USVs during neonatal opioid withdrawal. Methods We employed a third trimester-approximate opioid exposure model, where neonatal inbred FVB/NJ pups were injected twice-daily with morphine (10mg/kg, s.c.) or saline (0.9%, 20 ul/g, s.c.) from postnatal day(P) 1 to P14. This protocol induces reduced weight gain, hypothermia, thermal hyperalgesia, and increased USVs during spontaneous morphine withdrawal. Results On P14, there were increased USV emissions and altered USV syllables during withdrawal, including an increase in Complex 3 syllables in FVB/NJ females (but not males). Brainstem bulk mRNA sequencing revealed an upregulation of the kappa opioid receptor (Oprk1), which contributes to withdrawal-induced dysphoria. The kappa opioid receptor (KOR) antagonist, nor-BNI (30 mg/kg, s.c.), significantly reduced USVs in FVB/NJ females, but not males during spontaneous morphine withdrawal. Furthermore, the KOR agonist, U50,488h (0.625 mg/kg, s.c.), was sufficient to increase USVs on P10 (both sexes) and P14 (females only) in FVB/NJ mice. Conclusions We identified an elevated USV syllable, Complex 3, and a female-specific recruitment of the dynorphin/KOR system in increased USVs associated with neonatal opioid withdrawal severity.
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Affiliation(s)
- Kelly K. Wingfield
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- T32 Biomolecular Pharmacology Training Program, Boston University Chobanian & Avedisian School of Medicine, Boston, MA USA
| | - Teodora Misic
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Kaahini Jain
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Carly S. McDermott
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Nalia M. Abney
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Kayla T. Richardson
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- Post-Baccalaureate Research Education Program, Boston University Chobanian & Avedisian School of Medicine
| | | | - Jacob A. Beierle
- T32 Biomolecular Pharmacology Training Program, Boston University Chobanian & Avedisian School of Medicine, Boston, MA USA
- Transformative Training Program in Addiction Science, Boston University Chobanian & Avedisian School of Medicine
| | - Sophia A. Miracle
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- Graduate Program for Neuroscience, Boston University, Boston, MA USA
| | - Emma J. Sandago
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Britahny M. Baskin
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- T32 Training Program on Development of Medications for Substance Use Disorders Fellowship, Center for Drug Discovery, Northeastern University
| | - William B. Lynch
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- Transformative Training Program in Addiction Science, Boston University Chobanian & Avedisian School of Medicine
- Graduate Program for Neuroscience, Boston University, Boston, MA USA
| | - Kristyn N. Borrelli
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
- T32 Biomolecular Pharmacology Training Program, Boston University Chobanian & Avedisian School of Medicine, Boston, MA USA
- Transformative Training Program in Addiction Science, Boston University Chobanian & Avedisian School of Medicine
- Graduate Program for Neuroscience, Boston University, Boston, MA USA
| | - Emily J. Yao
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
| | - Elisha M. Wachman
- Department of Pediatrics, Boston University Chobanian & Avedisian School of Medicine, Boston Medical Center, Boston MA USA
| | - Camron D. Bryant
- Laboratory of Addiction Genetics, Center for Drug Discovery, Department of Pharmaceutical Sciences, Northeastern University, Boston, MA USA
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Hadaya L, Vanes L, Karolis V, Kanel D, Leoni M, Happé F, Edwards AD, Counsell SJ, Batalle D, Nosarti C. Distinct Neurodevelopmental Trajectories in Groups of Very Preterm Children Screening Positively for Autism Spectrum Conditions. J Autism Dev Disord 2024; 54:256-269. [PMID: 36273367 DOI: 10.1007/s10803-022-05789-4] [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] [Accepted: 10/09/2022] [Indexed: 10/24/2022]
Abstract
Very preterm (VPT; < 33 weeks' gestation) toddlers screening positively for autism spectrum conditions (ASC) may display heterogenous neurodevelopmental trajectories. Here we studied neonatal brain volumes and childhood ASC traits evaluated with the Social Responsiveness Scale (SRS-2) in VPT-born toddlers (N = 371; median age 20.17 months) sub-divided into three groups based on their Modified-Checklist for Autism in Toddlers scores. These were: those screening positively failing at least 2 critical items (critical-positive); failing any 3 items, but less than 2 critical items (non-critical-positive); and screening negatively. Critical-positive scorers had smaller neonatal cerebellar volumes compared to non-critical-positive and negative scorers. However, both positive screening groups exhibited higher childhood ASC traits compared to the negative screening group, suggesting distinct aetiological trajectories associated with ASC outcomes.
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Affiliation(s)
- Laila Hadaya
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
- Department of Child and Adolescent Psychiatry, Institute of Psychiatry Psychology and Neuroscience, King's College London, 16 De Crespigny Park, London, SE5 8AF, UK
| | - Lucy Vanes
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
- Department of Child and Adolescent Psychiatry, Institute of Psychiatry Psychology and Neuroscience, King's College London, 16 De Crespigny Park, London, SE5 8AF, UK
| | - Vyacheslav Karolis
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
- Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, OX3 9DU, UK
| | - Dana Kanel
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
- Department of Child and Adolescent Psychiatry, Institute of Psychiatry Psychology and Neuroscience, King's College London, 16 De Crespigny Park, London, SE5 8AF, UK
| | - Marguerite Leoni
- Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry Psychology and Neuroscience, King's College London, London, SE5 8AF, UK
| | - Francesca Happé
- Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry Psychology and Neuroscience, King's College London, London, SE5 8AF, UK
| | - A David Edwards
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
| | - Serena J Counsell
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
| | - Dafnis Batalle
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK
- Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry Psychology and Neuroscience, King's College London, London, SE5 8AF, UK
| | - Chiara Nosarti
- Centre for the Developing Brain, Department of Perinatal Imaging and Health, School of Biomedical Engineering and Imaging Sciences, King's College London, London, SE1 7EH, UK.
- Department of Child and Adolescent Psychiatry, Institute of Psychiatry Psychology and Neuroscience, King's College London, 16 De Crespigny Park, London, SE5 8AF, UK.
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Al-Beltagi M. Pre-autism: What a paediatrician should know about early diagnosis of autism. World J Clin Pediatr 2023; 12:273-294. [PMID: 38178935 PMCID: PMC10762597 DOI: 10.5409/wjcp.v12.i5.273] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/10/2023] [Revised: 09/07/2023] [Accepted: 09/25/2023] [Indexed: 12/08/2023] Open
Abstract
Autism, also known as an autism spectrum disorder, is a complex neurodevelopmental disorder usually diagnosed in the first three years of a child's life. A range of symptoms characterizes it and can be diagnosed at any age, including adolescence and adulthood. However, early diagnosis is crucial for effective management, prognosis, and care. Unfortunately, there are no established fetal, prenatal, or newborn screening programs for autism, making early detection difficult. This review aims to shed light on the early detection of autism prenatally, natally, and early in life, during a stage we call as "pre-autism" when typical symptoms are not yet apparent. Some fetal, neonatal, and infant biomarkers may predict an increased risk of autism in the coming baby. By developing a biomarker array, we can create an objective diagnostic tool to diagnose and rank the severity of autism for each patient. These biomarkers could be genetic, immunological, hormonal, metabolic, amino acids, acute phase reactants, neonatal brainstem function biophysical activity, behavioral profile, body measurements, or radiological markers. However, every biomarker has its accuracy and limitations. Several factors can make early detection of autism a real challenge. To improve early detection, we need to overcome various challenges, such as raising community awareness of early signs of autism, improving access to diagnostic tools, reducing the stigma attached to the diagnosis of autism, and addressing various culturally sensitive concepts related to the disorder.
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Affiliation(s)
- Mohammed Al-Beltagi
- Department of Pediatric, Faculty of Medicine, Tanta University, Tanta 31511, Algahrbia, Egypt
- Department of Pediatric, University Medical Center, King Abdulla Medical City, Arabian Gulf University, Dr. Sulaiman Al Habib Medical Group, Manama 26671, Manama, Bahrain
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Transient hearing abnormalities precede social deficits in a mouse model of autism. Behav Brain Res 2023; 437:114149. [PMID: 36206820 DOI: 10.1016/j.bbr.2022.114149] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2022] [Revised: 09/30/2022] [Accepted: 10/03/2022] [Indexed: 11/13/2022]
Abstract
Hearing abnormalities are important symptoms of autism spectrum disorders (ASDs), a neurological and developmental disorder. However, the characteristics of hearing abnormalities associated with ASD during development have not been fully investigated. We found that in Shank3B knockout mice (a high-confidence mouse model of ASD), transient hearing abnormalities can be found in auditory brainstem response, auditory cortical activity, as well as acoustic startle response. More importantly, all hearing abnormalities at 4 weeks were most prominent and preceded the onset of social deficits at 6 weeks. These hearing abnormalities gradually recovered with age. In addition, analysis of ABR data at 4 weeks using Support Vector Machine (SVM) can faithfully predict the genotype of mice with an accuracy of 85.71%. These findings not only revealed hearing changes in Shank3B knockout autistic-like mice during development, but also suggested that hearing abnormalities could potentially be used as an early and effective indicator of ASD risk.
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8
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Burstein O, Geva R. The Brainstem-Informed Autism Framework: Early Life Neurobehavioral Markers. Front Integr Neurosci 2021; 15:759614. [PMID: 34858145 PMCID: PMC8631363 DOI: 10.3389/fnint.2021.759614] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2021] [Accepted: 10/18/2021] [Indexed: 12/27/2022] Open
Abstract
Autism spectrum disorders (ASD) have long-term implications on functioning at multiple levels. In this perspective, we offer a brainstem-informed autism framework (BIAF) that traces the protracted neurobehavioral manifestations of ASD to early life brainstem dysfunctions. Early life brainstem-mediated markers involving functions of autonomic/arousal regulation, sleep-wake homeostasis, and sensorimotor integration are delineated. Their possible contributions to the early identification of susceptible infants are discussed. We suggest that the BIAF expands our multidimensional understanding of ASD by focusing on the early involvement of brainstem systems. Importantly, we propose an integrated BIAF screener that brings about the prospect of a sensitive and reliable early life diagnostic scheme for weighing the risk for ASD. The BIAF screener could provide clinicians substantial gains in the future and may carve customized interventions long before the current DSM ASD phenotype is manifested using dyadic co-regulation of brainstem-informed autism markers.
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Affiliation(s)
- Or Burstein
- Department of Psychology, Bar-Ilan University, Ramat Gan, Israel
| | - Ronny Geva
- Department of Psychology, Bar-Ilan University, Ramat Gan, Israel
- Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat Gan, Israel
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9
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Wass SV. The origins of effortful control: How early development within arousal/regulatory systems influences attentional and affective control. DEVELOPMENTAL REVIEW 2021. [DOI: 10.1016/j.dr.2021.100978] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/27/2022]
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10
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Dean B, Ginnell L, Boardman JP, Fletcher-Watson S. Social cognition following preterm birth: A systematic review. Neurosci Biobehav Rev 2021; 124:151-167. [PMID: 33524414 DOI: 10.1016/j.neubiorev.2021.01.006] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/12/2020] [Revised: 12/22/2020] [Accepted: 01/04/2021] [Indexed: 01/15/2023]
Abstract
Social cognitive abilities are affected by preterm birth, but pathways to, and risk factors for this outcome are not well mapped. We examined direct assessment tasks including objective coding of parent-child play to chart social development in infancy and pre-school years. A systematic search and data-extraction procedure yielded seventy-nine studies (4930 preterm and 2109 term children, aged birth - five years), for inclusion. We detected a pattern of reduced social attention in the first 12 months of life with evidence of reduced performance in social cognitive tasks later in the preschool years. However, we did not identify a consistent, distinctive preterm social phenotype in early life. Instead, the interactive behaviour of preterm infants reflects factors from outside the social cognitive domain, such as attention, language, and socioeconomic status. By combining data across samples and measures we revealed the role of domain-general skills, which may in future prove fruitful intervention targets.
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Affiliation(s)
- Bethan Dean
- MRC Centre for Reproductive Health, University of Edinburgh, UK
| | - Lorna Ginnell
- MRC Centre for Reproductive Health, University of Edinburgh, UK
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Zivan M, Morag I, Yarmolovsky J, Geva R. Hyper-Reactivity to Salience Limits Social Interaction Among Infants Born Pre-term and Infant Siblings of Children With ASD. Front Psychiatry 2021; 12:646838. [PMID: 34054606 PMCID: PMC8160104 DOI: 10.3389/fpsyt.2021.646838] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/05/2021] [Accepted: 04/12/2021] [Indexed: 12/13/2022] Open
Abstract
The ability to engage attention with selected stimuli is essential for infants to explore the world and process information relating to their surroundings. There are two main populations with a higher risk to develop attentional and social deficits whose deficits may arise from difficulties in regulating attention to salient cues: (1) siblings of children diagnosed with Autism; and (2) infants who were born pre-term. This study investigated infants' (N = 97) attention-engagement and pupil-dilation (PD) at 9 months of age, using a gaze-contingent paradigm and a structured social interaction. Specifically, we explored attention to stimuli with simple salient features (e.g., clear defined shapes, colors, and motions) vs. more complex non-social cues (amorphous shapes, colors, and motions) and social interaction in typically developing infants (TD, N = 25) and among two groups of infants at-risk to develop social difficulties (pre-terms, N = 56; siblings of children with Autism, N = 16). Findings show that the two risk groups preferred stimuli with simple features (F = 11.306, p < 0.001), accompanied by increased PD (F = 6.6, p < 0.001). Specifically, pre-term infants showed increased PD toward simple vs. complex stimuli (p < 0.001), while siblings showed a pervasive hyper-arousal to both simple and complex stimuli. Infants in the TD group preferred complex stimuli with no change in PD. Finally, the preference for the simple stimulus mediated the relationship between increased risk for social difficulties and decreased engagement duration in face-to-face interaction with the experimenter. Results suggest that activation of the attention-salience network shapes social abilities at infancy. Further, hyper-reactivity to salient stimuli limits social interaction among infants born pre-term and siblings of children with ASD.
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Affiliation(s)
- Michal Zivan
- The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel
| | - Iris Morag
- Assaf Harofeh Medical Center, Zerifin, Israel.,Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
| | - Jessica Yarmolovsky
- The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel.,The Department of Psychology, Bar Ilan University, Ramat Gan, Israel
| | - Ronny Geva
- The Gonda Multidisciplinary Brain Research Center, Bar Ilan University, Ramat Gan, Israel.,The Department of Psychology, Bar Ilan University, Ramat Gan, Israel
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12
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Corrigan FM, Christie-Sands J. An innate brainstem self-other system involving orienting, affective responding, and polyvalent relational seeking: Some clinical implications for a "Deep Brain Reorienting" trauma psychotherapy approach. Med Hypotheses 2019; 136:109502. [PMID: 31794877 DOI: 10.1016/j.mehy.2019.109502] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2019] [Revised: 11/11/2019] [Accepted: 11/16/2019] [Indexed: 11/29/2022]
Abstract
Underlying any complex relational intersubjectivity there is an inherent urge to connect, to have proximity, to engage in an experience of interpersonal contact. The hypothesis set out here is that this most basic urge to connect is dependent on circuits based in three main components: the midbrain superior colliculi (SC), the midbrain periaqueductal gray (PAG), and the mesolimbic and mesocortical dopamine systems originating in the midbrain ventral tegmental area. Firstly, there is orienting towards or away from interpersonal contact, dependent on approach and/or defensive/withdrawal areas of the SC. Secondly, there is an affective response to the contact, mediated by the PAG. Thirdly, there is an associated, affectively-loaded, seeking drive based in the mesolimbic and mesocortical dopamine systems. The neurochemical milieu of these dopaminergic systems is responsive to environmental factors, creating the possibility of multiple states of functioning with different affective valences, a polyvalent range of subjectively positive and negative experiences. The recognition of subtle tension changes in skeletal muscles when orienting to an affectively significant experience or event has clinical implications for processing of traumatic memories, including those of a relational/interpersonal nature. Sequences established at the brainstem level can underlie patterns of attachment responding that repeat over many years in different contexts. The interaction of the innate system for connection with that for alarm, through circuits based in the locus coeruleus, and that for defence, based in circuits through the PAG, can lay down deep patterns of emotional and energetic responses to relational stimuli. There may be simultaneous sequences for attachment approach and defensive aggression underlying relational styles that are so deep as to be seen as personality characteristics, for example, of borderline type. A clinical approach derived from these hypotheses, Deep Brain Reorienting, is briefly outlined as it provides a way to address the somatic residues of adverse interpersonal interactions underlying relational patterns and also the residual shock and horror of traumatic experiences. We suggest that the innate alarm system involving the SC and the locus coeruleus can generate a pre-affective shock while an affective shock can arise from excessive stimulation of the PAG. Clinically significant residues can be accessed through careful, mindful, attention to orienting-tension-affect-seeking sequences when the therapist and the client collaborate on eliciting and describing them.
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Affiliation(s)
- F M Corrigan
- Trauma Psychotherapy Scotland, 15 Newton Terrace, Glasgow G3 7PJ, United Kingdom.
| | - J Christie-Sands
- Trauma Psychotherapy Scotland, 15 Newton Terrace, Glasgow G3 7PJ, United Kingdom
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Wass SV, Smith CG, Daubney KR, Suata ZM, Clackson K, Begum A, Mirza FU. Influences of environmental stressors on autonomic function in 12-month-old infants: understanding early common pathways to atypical emotion regulation and cognitive performance. J Child Psychol Psychiatry 2019; 60:1323-1333. [PMID: 31259425 DOI: 10.1111/jcpp.13084] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 05/22/2019] [Indexed: 12/19/2022]
Abstract
BACKGROUND Previous research has suggested that children exposed to more early-life stress show worse mental health outcomes and impaired cognitive performance in later life, but the mechanisms subserving these relationships remain poorly understood. METHOD Using miniaturised microphones and physiological arousal monitors (electrocardiography, heart rate variability and actigraphy), we examined for the first time infants' autonomic reactions to environmental stressors (noise) in the home environment, in a sample of 82 12-month-old infants from mixed demographic backgrounds. The same infants also attended a laboratory testing battery where attention- and emotion-eliciting stimuli were presented. We examined how children's environmental noise exposure levels at home related to their autonomic reactivity and to their behavioural performance in the laboratory. RESULTS Individual differences in total noise exposure were independent of other socioeconomic and parenting variables. Children exposed to higher and more rapidly fluctuating environmental noise showed more unstable autonomic arousal patterns overall in home settings. In the laboratory testing battery, this group showed more labile and short-lived autonomic changes in response to novel attention-eliciting stimuli, along with reduced visual sustained attention. They also showed increased arousal lability in response to an emotional stressor. CONCLUSIONS Our results offer new insights into the mechanisms by which environmental noise exposure may confer increased risk of adverse mental health and impaired cognitive performance during later life.
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Affiliation(s)
- Sam V Wass
- School of Psychology, University of East London, London, UK
| | - Celia G Smith
- Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
| | | | - Zeynep M Suata
- Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
| | - Kaili Clackson
- Department of Experimental Psychology, University of Cambridge, Cambridge, UK
| | - Abdul Begum
- School of Psychology, University of East London, London, UK
| | - Farhan U Mirza
- School of Health Professions, University of Plymouth, Plymouth, UK
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14
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M Reyes L, Jaekel J, Wolke D. Effects of Gestational Age and Early Parenting on Children's Social Inhibition at 6 Years. CHILDREN (BASEL, SWITZERLAND) 2019; 6:E81. [PMID: 31261690 PMCID: PMC6678926 DOI: 10.3390/children6070081] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 05/01/2019] [Revised: 06/18/2019] [Accepted: 06/25/2019] [Indexed: 11/25/2022]
Abstract
Preterm birth (<37 weeks' gestation) has been associated with problems in social functioning. Whether social inhibition is specifically related to preterm birth and whether early parenting may protect against social inhibition difficulties is unknown. To explore effects of gestational age and early parent-infant relationships on social inhibition, 1314 children born at 26-41 weeks gestational age were studied as part of the prospective Bavarian Longitudinal Study. Early parent-infant relationship quality was assessed postnatally with the parent-infant relationship index. Social inhibition was assessed at age 6 years using an experimental procedure, in which nonverbal and verbal responses were coded into social inhibition categories (disinhibited, normally responsive, inhibited). Multinomial logistic regressions indicated that children with lower gestational age showed more socially disinhibited (nonverbal: OR = 1.27 [95% CI = 1.17-1.40], verbal: OR = 1.23 [95% CI 1.13-1.35]) and inhibited (nonverbal: OR = 1.21 [95% CI = 1.11-1.32], verbal: OR = 1.11 [95% CI = 1.01-1.21]) responses. Good early parent-infant relationships were associated with less verbal disinhibition (OR = 0.70 [95% CI = 0.52-0.93]). Findings suggest that children with lower gestational age are at greater risk to be both socially inhibited and disinhibited. Early parenting affected risk of abnormal social responses. Supporting early parent-infant relationships may reduce preterm children's risk for social difficulties.
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Affiliation(s)
- Lucia M Reyes
- Department of Child and Family Studies, The University of Tennessee, Knoxville, TN 37996, USA
| | - Julia Jaekel
- Department of Child and Family Studies, The University of Tennessee, Knoxville, TN 37996, USA
- Department of Psychology, University of Warwick, Coventry CV47AL, UK
| | - Dieter Wolke
- Department of Psychology, University of Warwick, Coventry CV47AL, UK.
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15
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Mirza R, Sharma B. Benefits of Fenofibrate in prenatal valproic acid-induced autism spectrum disorder related phenotype in rats. Brain Res Bull 2019; 147:36-46. [PMID: 30769127 DOI: 10.1016/j.brainresbull.2019.02.003] [Citation(s) in RCA: 53] [Impact Index Per Article: 8.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/08/2018] [Revised: 01/29/2019] [Accepted: 02/06/2019] [Indexed: 12/12/2022]
Abstract
Autism Spectrum Disorder (ASD) is a neurodevelopmental disorder with two major behavioral symptoms i.e. repetitive behavior and social-communication impairment. The unknown etiology of ASD is responsible for the difficulty in identifying the possible therapeutic modulators for ASD. Valproic acid (VPA) is an anticonvulsant drug in both human and rodents with teratogenic effects during pregnancy. Therefore, prenatal exposure of VPA induced autism spectrum disorder like phenotypes in both human and rodents. Peroxisome proliferator-activated receptor-alpha (PPAR-α) is widely localized in the brain. This research investigates the utility of fenofibrate, a selective agonist of PPAR-α in prenatal VPA-induced experimental ASD in Wistar rats. The prenatal VPA has induced social impairment (three chambers social behavior apparatus), repetitive behavior (Y-maze), hyperlocomotion (actophotometer), anxiety (elevated plus maze) and low exploratory activity (hole board test). Also, prenatal VPA treated rats have shown higher levels of oxidative stress (increased in thiobarbituric acid reactive species and decreased in reduced glutathione level) and inflammation (increased in interleukin-6, tumor necrosis factor-α and decreased in interleukin-10) in the cerebellum, brainstem and prefrontal cortex. Treatment with fenofibrate significantly attenuated prenatal VPA-induced social impairment, repetitive behavior, hyperactivity, anxiety, and low exploratory activity. Furthermore, fenofibrate also decreased the prenatal VPA-induced oxidative stress and inflammation in brain regions. Hence, it may be concluded that fenofibrate may provide neurobehavioral and biochemical benefits in prenatal VPA-induced autism phenotypes in rats.
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Affiliation(s)
- Roohi Mirza
- Department of Pharmacology, Amity Institute of Pharmacy, Amity University Uttar Pradesh, India
| | - Bhupesh Sharma
- Department of Pharmacology, Amity Institute of Pharmacy, Amity University Uttar Pradesh, India; CNS Pharmacology, Conscience Research, Delhi, India.
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16
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Mirza R, Sharma B. Selective modulator of peroxisome proliferator-activated receptor-α protects propionic acid induced autism-like phenotypes in rats. Life Sci 2018; 214:106-117. [PMID: 30366038 DOI: 10.1016/j.lfs.2018.10.045] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/23/2018] [Revised: 10/12/2018] [Accepted: 10/22/2018] [Indexed: 01/15/2023]
Abstract
AIMS The present study investigated the neuropharmacological role of PPAR-α modulator, fenofibrate in postnatal-propionic acid induced symptomatology related with autism spectrum disorders (ASD) in Wistar rats. MAIN METHODS The propionic acid (250 mg/kg, p.o.) was administered to rats from postnatal 21st day to 23rd day to induce autism-related neurobehavioral and neurobiochemical alterations in rats. Then, rats were treated with fenofibrate (100 mg/kg and 200 mg/kg, orally) from postnatal 24th day till 48th day. The social behavior (three chambers social testing apparatus), repetitive behavior (Y-maze), locomotor activity (actophotometer), anxiety (elevated plus maze) and exploratory behavior (hole board test) were assessed. Biochemically, oxidative stress (thiobarbituric acid reactive species and reduced glutathione level) and neuroinflammation (interleukin-6, tumor necrosis factor-α and interleukin-10) were evaluated in the cerebellum, brainstem and prefrontal cortex of rats. KEY FINDINGS Propionic acid-treated rats showed social impairment, repetitive behavior, hyperlocomotion, anxiety and low exploratory activity. Also, these animals showed higher levels of oxidative stress (increased in thiobarbituric acid reactive species and decreased in reduced glutathione level) as well as inflammation (increased in interleukin-6, tumor necrosis factor-α and decreased in interleukin-10) and inflammation in aforementioned brain-regions. Treatment with fenofibrate significantly attenuated the propionic acid induced-social impairment, repetitive behavior, hyperactivity, anxiety and low exploratory activity. Furthermore, fenofibrate also reduced the oxidative stress and neuroinflammation in propionic acid-treated rats. SIGNIFICANCE A selective PPAR-α agonist, fenofibrate provides neurobehavioral and neurobiochemical benefits in postnatal-propionic acid induced autism-related phenotype in rats. Thus, fenofibrate may further be studied for its possible benefits in ASD symptoms.
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Affiliation(s)
- Roohi Mirza
- Department of Pharmacology, Amity Institute of Pharmacy, Amity University Uttar Pradesh, India
| | - Bhupesh Sharma
- Department of Pharmacology, Amity Institute of Pharmacy, Amity University Uttar Pradesh, India; CNS Pharmacology, Conscience Research, Delhi, India.
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17
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Dadalko OI, Travers BG. Evidence for Brainstem Contributions to Autism Spectrum Disorders. Front Integr Neurosci 2018; 12:47. [PMID: 30337860 PMCID: PMC6180283 DOI: 10.3389/fnint.2018.00047] [Citation(s) in RCA: 42] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/24/2018] [Accepted: 09/18/2018] [Indexed: 12/27/2022] Open
Abstract
Autism spectrum disorder (ASD) is a neurodevelopmental condition that affects one in 59 children in the United States. Although there is a mounting body of knowledge of cortical and cerebellar contributions to ASD, our knowledge about the early developing brainstem in ASD is only beginning to accumulate. Understanding how brainstem neurotransmission is implicated in ASD is important because many of this condition’s sensory and motor symptoms are consistent with brainstem pathology. Therefore, the purpose of this review was to integrate epidemiological, behavioral, histological, neuroimaging, and animal evidence of brainstem contributions to ASD. Because ASD is a neurodevelopmental condition, we examined the available data through a lens of hierarchical brain development. The review of the literature suggests that developmental alterations of the brainstem could have potential cascading effects on cortical and cerebellar formation, ultimately leading to ASD symptoms. This view is supported by human epidemiology findings and data from animal models of ASD, showing that perturbed development of the brainstem substructures, particularly during the peak formation of the brainstem’s monoaminergic centers, may relate to ASD or ASD-like behaviors. Furthermore, we review evidence from human histology, psychophysiology, and neuroimaging suggesting that brainstem development and maturation may be atypical in ASD and may be related to key ASD symptoms, such as atypical sensorimotor features and social responsiveness. From this review there emerges the need of future research to validate early detection of the brainstem-based somatosensory and psychophysiological behaviors that emerge in infancy, and to examine the brainstem across the life span, while accounting for age. In all, there is preliminary evidence for brainstem involvement in ASD, but a better understanding of the brainstem’s role would likely pave the way for earlier diagnosis and treatment of ASD.
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Affiliation(s)
- Olga I Dadalko
- Motor and Brain Development Lab, Waisman Center, University of Wisconsin-Madison, Madison, WI, United States
| | - Brittany G Travers
- Motor and Brain Development Lab, Occupational Therapy Program in the Department of Kinesiology, University of Wisconsin-Madison, Madison, WI, United States
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18
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Wass SV. How orchids concentrate? The relationship between physiological stress reactivity and cognitive performance during infancy and early childhood. Neurosci Biobehav Rev 2018; 90:34-49. [DOI: 10.1016/j.neubiorev.2018.03.029] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/07/2017] [Revised: 03/26/2018] [Accepted: 03/30/2018] [Indexed: 12/19/2022]
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19
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Association of Sleep and Circadian Activity Rhythm with Emotional Face Processing among 12-month-old Infants. Sci Rep 2018; 8:3200. [PMID: 29453399 PMCID: PMC5816664 DOI: 10.1038/s41598-018-21448-0] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2017] [Accepted: 01/29/2018] [Indexed: 01/08/2023] Open
Abstract
Sleep and circadian rhythmicity both play an important role in human’s cognitive functioning, yet the way in which early development of sleep and circadian rhythm affects cognitive processes and social learning in infants remains less understood. We examined the association of sleep and circadian activity rhythm (CAR) with face and emotional information processing in 12-month old infants. Face processing was measured by eye tracking, whereby infants’ scanning patterns and pupil dilations were calculated when they were presented with neutral, pleasant and unpleasant faces. Infants with better sleep quality (i.e., less waking after sleep onset) and lower sleep-wake pattern variability (i.e., higher inter-daily stability) exhibited a higher eyes over mouth fixation ratio (EMR). Infants with longer total sleep time showed larger pupil diameter changes in response to emotional facial expressions, more closely resembling the responses of adults. Our findings suggest the role of sleep and circadian rhythm in waking cognition and have implications for understanding the early development of social learning in young children.
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20
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Geva R, Dital A, Ramon D, Yarmolovsky J, Gidron M, Kuint J. Brainstem as a developmental gateway to social attention. J Child Psychol Psychiatry 2017; 58:1351-1359. [PMID: 28504308 DOI: 10.1111/jcpp.12746] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 02/24/2017] [Indexed: 01/01/2023]
Abstract
BACKGROUND Evolution preserves social attention due to its key role in supporting survival. Humans are attracted to social cues from infancy, but the neurobiological mechanisms for the development of social attention are unknown. An evolutionary-based, vertical-hierarchical theoretical model of self-regulation suggests that neonatal brainstem inputs are key for the development of well-regulated social attention. METHODS Neonates born preterm (N = 44, GA 34 w.) were recruited and diagnosed at birth as a function of their auditory brainstem evoked responses (ABR). Participants enrolled in a prospective 8-year-long, double-blind, follow-up study comparing participants with brainstem dysfunctions and well-matched controls. Groups had comparable fetal, neonatal, and familial characteristics. Methods incorporated EEG power analysis and gaze tracking during the Attention Network Test (ANT, four cue types, and two targets) and a Triadic Gaze Engagement task (TGE, three social cue levels). RESULTS Results showed that neonatal brainstem compromise is related to long-term changes in Alpha- and Theta-band power asymmetries (p < .034, p < .016, respectively), suggesting suppressed bottom-up input needed to alert social attention. Gaze tracking indicated dysregulated arousal-modulated attention (p < .004) and difficulty in gaze engagement to socially neutral compared to nonsocial cues (p < .012). CONCLUSIONS Integrating models of Autism and cross-species data with current long-term follow-up of infants with discrete neonatal brainstem dysfunction suggests neonatal brainstem input as a gateway for bottom-up regulation of social attention.
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Affiliation(s)
- Ronny Geva
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel.,The Gonda Multidisciplinary Brain Research Center Bar Ilan University, Ramat Gan, Israel
| | - Ayelet Dital
- The Gonda Multidisciplinary Brain Research Center Bar Ilan University, Ramat Gan, Israel
| | - Dan Ramon
- Psychology Department, Ashkelon College, Ashkelon, Israel
| | - Jessica Yarmolovsky
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel.,The Gonda Multidisciplinary Brain Research Center Bar Ilan University, Ramat Gan, Israel
| | - Maor Gidron
- Department of Psychology, Bar Ilan University, Ramat Gan, Israel.,The Gonda Multidisciplinary Brain Research Center Bar Ilan University, Ramat Gan, Israel
| | - Jacob Kuint
- Neonatology Department, Sheba Medical Center, Ramat Gan, Israel.,Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
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21
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Wass SV, Clackson K, de Barbaro K. Temporal dynamics of arousal and attention in 12-month-old infants. Dev Psychobiol 2016; 58:623-39. [DOI: 10.1002/dev.21406] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/24/2015] [Accepted: 02/25/2016] [Indexed: 11/11/2022]
Affiliation(s)
- S. V. Wass
- University of East London; Water London London, E15 4LZ
- University of Cambridge, Free School Lane; Cambridge, CB2 3RQ United Kingdom
| | - K. Clackson
- University of Cambridge, Free School Lane; Cambridge, CB2 3RQ United Kingdom
| | - K. de Barbaro
- Georgia Institute of Technology; North Ave NW Atlanta GA 30332
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22
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Abstract
OBJECTIVE Children with sleep disorders tend to experience attention problems, yet little is known about the relationship between sleep and attention in early development. This prospective follow-up study investigated the longitudinal relationships between neonatal sleep, attention, and distraction in infants born preterm. METHOD We used actigraphy and sleep-wake diaries in the neonatal intensive care unit (NICU, N = 65), attention orienting in a visual-recognition-memory task (VRM) at age 4 months, and structured observation of attention and distractibility at age 18 months. RESULTS Infants with poorer neonatal sleep (n = 31) exhibited longer first gaze durations in the VRM at 4 months and longer distraction episodes at 18 months relative to neonatal controls who slept well (p < .01). Hierarchical regression models support relations between neonatal sleep and gaze behavior at 4 months and distractibility at 18 months; moreover, alterations in orienting attention at 4 months predicted the likelihood of being distracted during the second year of life. CONCLUSION Findings underscore the importance of early sleep-wake and attention regulation in the development of distraction in infants born preterm.
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Affiliation(s)
- Ronny Geva
- Department of Psychology, Bar-Ilan University, Ramat Gan, Israel
| | - Hagit Yaron
- Department of Psychology, Bar-Ilan University, Ramat Gan, Israel
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23
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Miron O, Ari-Even Roth D, Gabis LV, Henkin Y, Shefer S, Dinstein I, Geva R. Prolonged auditory brainstem responses in infants with autism. Autism Res 2015; 9:689-95. [PMID: 26477791 PMCID: PMC5057307 DOI: 10.1002/aur.1561] [Citation(s) in RCA: 38] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/16/2015] [Accepted: 08/18/2015] [Indexed: 01/15/2023]
Abstract
Numerous studies have attempted to identify early physiological abnormalities in infants and toddlers who later develop autism spectrum disorder (ASD). One potential measure of early neurophysiology is the auditory brainstem response (ABR), which has been reported to exhibit prolonged latencies in children with ASD. We examined whether prolonged ABR latencies appear in infancy, before the onset of ASD symptoms, and irrespective of hearing thresholds. To determine how early in development these differences appear, we retrospectively examined clinical ABR recordings of infants who were later diagnosed with ASD. Of the 118 children in the participant pool, 48 were excluded due to elevated ABR thresholds, genetic aberrations, or old testing age, leaving a sample of 70 children: 30 of which were tested at 0–3 months, and 40 were tested at toddlerhood (1.5–3.5 years). In the infant group, the ABR wave‐V was significantly prolonged in those who later developed ASD as compared with case‐matched controls (n = 30). Classification of infants who later developed ASD and case‐matched controls using this measure enabled accurate identification of ASD infants with 80% specificity and 70% sensitivity. In the group of toddlers with ASD, absolute and interpeak latencies were prolonged compared to clinical norms. Findings indicate that ABR latencies are significantly prolonged in infants who are later diagnosed with ASD irrespective of their hearing thresholds; suggesting that abnormal responses might be detected soon after birth. Further research is needed to determine if ABR might be a valid marker for ASD risk. Autism Res2016, 9: 689–695. © 2015 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research
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Affiliation(s)
- Oren Miron
- Department of Psychology, Ben-Gurion University of the Negev, Beer Sheva, Israel.,Developmental Neuropsychology Laboratory, The Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat Gan, Israel.,Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer Sheva, Israel
| | - Daphne Ari-Even Roth
- Hearing, Speech and Language Center, Sheba Medical Center, Ramat Gan, Israel.,Department of Communication Disorders, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
| | - Lidia V Gabis
- The Weinberg Child Development Center, Safra Children's Hospital, Sheba Medical Center, Ramat Gan, Israel
| | - Yael Henkin
- Hearing, Speech and Language Center, Sheba Medical Center, Ramat Gan, Israel.,Department of Communication Disorders, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
| | - Shahar Shefer
- The Weinberg Child Development Center, Safra Children's Hospital, Sheba Medical Center, Ramat Gan, Israel
| | - Ilan Dinstein
- Department of Psychology, Ben-Gurion University of the Negev, Beer Sheva, Israel.,Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer Sheva, Israel
| | - Ronny Geva
- Developmental Neuropsychology Laboratory, The Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat Gan, Israel.,Department of Psychology, Bar-Ilan University, Ramat Gan, Israel
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24
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Lev-Enacab O, Sher-Censor E, Einspieler C, Daube-Fishman G, Beni-Shrem S. The Quality of Spontaneous Movements of Preterm Infants: Associations with the Quality of Mother-Infant Interaction. INFANCY 2015. [DOI: 10.1111/infa.12096] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/30/2022]
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25
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Weber AM, Harrison TM. Maternal behavior and infant physiology during feeding in premature and term infants over the first year of life. Res Nurs Health 2014; 37:478-89. [PMID: 25223730 DOI: 10.1002/nur.21618] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 07/29/2014] [Indexed: 11/12/2022]
Abstract
Little is known about the relationship between maternal behavior and the stability of premature infants' physiologic responses during feeding. In a secondary data analysis, we examined relationships between quality of maternal behavior and cardiorespiratory physiology during feeding in 61 premature and 53 term infants at four times over the first year of life. Measures included heart rate (HR), respiratory rate (RR), and oxygen saturation; Child Feeding Skills Checklist; and Parent-Child Early Relational Assessment. Birthweight, gestational age, and neurodevelopmental risk were covariates. Quality of maternal behavior did not predict infants' physiologic response to feeding. However, birthweight was related to infant feeding physiology among all infants over the first year of life. Stress during fetal life, which may lead to impaired intrauterine growth and low birthweight, may have longitudinal effects on cardiorespiratory functioning of premature infants. Research is needed to further investigate the biological pathways by which maternal-infant interaction supports behavioral and physiologic feeding outcomes of premature infants.
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Affiliation(s)
- Ashley M Weber
- Doctoral Candidate, The Ohio State University College of Nursing, Columbus, Ohio
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26
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Geva R, Schreiber J, Segal-Caspi L, Markus-Shiffman M. Neonatal brainstem dysfunction after preterm birth predicts behavioral inhibition. J Child Psychol Psychiatry 2014; 55:802-10. [PMID: 24372410 DOI: 10.1111/jcpp.12188] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 11/11/2013] [Indexed: 11/30/2022]
Abstract
BACKGROUND Behavioral inhibition (BI), the tendency to withdraw or exhibit negative affect when experiencing stressful situations, is a major risk factor for the development of social anxiety. However, neonatal biologic origins of this progression are still unknown. Click here to enter text.This study aimed to extend frameworks of behavioral inhibition by exploring empirically the central role of neonatal brainstem electrophysiologic functions in the development of social disengagement and BI. METHODS Sixty-six preterm neonates (means ±SD: gestation age = 33.1 ± 1.22 weeks, birth weight = 1775 + 346.7 g; 51% female) participated in a prospective longitudinal study. The infants were tested within the first 2 weeks of postnatal life using an auditory brainstem-evoked response test. Based on the typicality of the major ABR wave latencies, waves I, III and V, neonates were divided into two groups (compromised, CBSF- with at least one component ≥1.5 SDs from the mean for the respective gestation age; normal, NBSF, with all components within 1.5 SD around the mean), and were enrolled in a prospective longitudinal follow-up study. This report extends previous work from 4 m by testing responses to socioemotional challenges during the Separation-Reunion paradigm at 12 m. RESULTS Results show that infants with neonatal CBSF were more susceptible to be classified as BI at 12 m (age corrected for prematurity) than infants with NBSF (66% vs. 40%, respectively). The most striking symptom in the CBSF group was a disability to initiate self-regulatory activities in response to a socioemotional challenge, resulting in frequent passivity/dependency (p < .001). Statistical regression analysis revealed that face-to-face gaze engagement at 4 m moderates the risk related to neonatal CBSF for the emergence of BI at 12 m, but did not overturn the emergence of BI. CONCLUSION Results support the hypothesis that neonatal brainstem dysfunction canalizes behavioral inhibition. These findings highlight, for the first time, the role of the early developing brainstem in later development of BI and in abilities to initiate self-regulatory behavior.
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Affiliation(s)
- Ronny Geva
- Department of Psychology, The Gonda Multidisciplinary Brain Research Center, Bar-Ilan University, Ramat Gan, Israel
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27
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Cohen IL, Gardner JM, Karmel BZ, Phan HTT, Kittler P, Gomez TR, Gonzalez MG, Lennon EM, Parab S, Barone A. Neonatal brainstem function and 4-month arousal-modulated attention are jointly associated with autism. Autism Res 2013; 6:11-22. [PMID: 23165989 PMCID: PMC3578986 DOI: 10.1002/aur.1259] [Citation(s) in RCA: 39] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/25/2012] [Accepted: 09/26/2012] [Indexed: 11/10/2022]
Abstract
The authors evaluated the contribution of initially abnormal neonatal auditory brainstem responses (ABRs) and 4-month arousal-modulated attention visual preference to later autism spectrum disorder (ASD) behaviors in neonatal intensive care unit (NICU) graduates. A longitudinal study design was used to compare NICU graduates with normal ABRs (n = 28) to those with initially abnormal ABRs (n = 46) that later resolved. At 4 months postterm age, visual preference (measured after feeding) for a random check pattern flashing at 1, 3, or 8 Hz and gestational age (GA) served as additional predictors. Outcome measures were PDD Behavior Inventory (PDDBI) scores at 3.4 years (standard deviation = 1.2), and developmental quotients (DQ) obtained around the same age with the Griffiths Mental Development Scales (GMDS). Preferences for higher rates of stimulation at 4 months were highly correlated with PDDBI scores (all P-values < 0.01) and the GMDS Hearing and Speech DQ, but only in those with initially abnormal ABRs. Effects were strongest for a PDDBI social competence measure most associated with a diagnosis of autism. For those with abnormal ABRs, increases in preference for higher rates of stimulation as infants were linked to nonlinear increases in severity of ASD at 3 years and to an ASD diagnosis. Abnormal ABRs were associated with later reports of repetitive and ritualistic behaviors irrespective of 4-month preference for stimulation. The joint occurrence of initially abnormal neonatal ABRs and preference for more stimulation at 4 months, both indices of early brainstem dysfunction, may be a marker for the development of autism in this cohort.
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Affiliation(s)
- Ira L Cohen
- Department of Psychology, New York State Institute for Basic Research in Developmental Disabilities, Staten Island, NY 10314, USA.
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28
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Gavrilov Y, Rotem S, Ofek R, Geva R. Socio-cultural effects on children's initiation of joint attention. Front Hum Neurosci 2012; 6:286. [PMID: 23112768 PMCID: PMC3480652 DOI: 10.3389/fnhum.2012.00286] [Citation(s) in RCA: 10] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/31/2012] [Accepted: 09/28/2012] [Indexed: 11/20/2022] Open
Abstract
Exchanging gazes with a social partner in response to an event in the environment is considered an effective means to direct attention, share affective experiences, and highlight a target in the environment. This behavior appears during infancy and plays an important role in children's learning and in shaping their socio-emotional development. It has been suggested that cultural values of the community affect socio-emotional development through attentional dynamics of social reference (Rogoff et al., 1993). Maturational processes of brain-circuits have been found to mediate socio-cultural learning and the behavioral manifestation of cultural norms starting at preschool age (Nelson and Guyer, 2011). The aim of the current study was to investigate the relations between cultural ecology levels and children's joint attention (JA). Initiation of JA bids was studied empirically as a function of the level of social load of the target toy (3 levels), the community level of adherence to traditional values (3 levels), parental education (2 levels), and gender. Sixty-two kindergarten aged children were enrolled in a structured toy-exploration task, during which they were presented with toys of various social loads, with social agents (i.e., mother and experimenter) present nearby, and non-social distracters presented intermittently. Measurements included the child's number of JA bids and the extent of positive affect. Analysis of variance indicated that the child's initiation of JA toward the social partner was affected by all levels of cultural ecology (i.e., toy's social load, adherence to tradition values, parental education, gender), thus supporting the study's hypotheses. The effects were such that overall, children, particularly girls' JA initiation was augmented in social toys and moderated by the socio-cultural variables. These results suggest that cultural ecology is related to children's JA, thereby scaffolding initiation of social sharing cues between children and adults. JA plays a role in adjusting children's internal representations of their respective ecological environment.
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Affiliation(s)
| | | | | | - Ronny Geva
- The Developmental Neuropsychology Lab, Department of Psychology, The Gonda Multidisciplinary Brain Research Center, Bar Ilan UniversityRamat Gan, Israel
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