An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy
Infancy represents a critical period during which thalamocortical brain connections develop and mature. Deviations in the maturation of thalamocortical connectivity are linked to neurodevelopmental disorders. There is a lack of early biomarkers to detect and localize neuromaturational deviations, wh...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-04-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811923000721 |
| _version_ | 1828037162773250048 |
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| author | Valeria Jaramillo Sarah F. Schoch Andjela Markovic Malcolm Kohler Reto Huber Caroline Lustenberger Salome Kurth |
| author_facet | Valeria Jaramillo Sarah F. Schoch Andjela Markovic Malcolm Kohler Reto Huber Caroline Lustenberger Salome Kurth |
| author_sort | Valeria Jaramillo |
| collection | DOAJ |
| description | Infancy represents a critical period during which thalamocortical brain connections develop and mature. Deviations in the maturation of thalamocortical connectivity are linked to neurodevelopmental disorders. There is a lack of early biomarkers to detect and localize neuromaturational deviations, which can be overcome with mapping through high-density electroencephalography (hdEEG) assessed in sleep. Specifically, slow waves and spindles in non-rapid eye movement (NREM) sleep are generated by the thalamocortical system, and their characteristics, slow wave slope and spindle density, are closely related to neuroplasticity and learning. Spindles are often subdivided into slow (11.0-13.0 Hz) and fast (13.5-16.0 Hz) frequencies, for which not only different functions have been proposed, but for which also distinctive developmental trajectories have been reported across the first years of life. Recent studies further suggest that information processing during sleep underlying sleep-dependent learning is promoted by the temporal coupling of slow waves and spindles, yet slow wave-spindle coupling remains unexplored in infancy. Thus, we evaluated three potential biomarkers: 1) slow wave slope, 2) spindle density, and 3) the temporal coupling of slow waves with spindles. We use hdEEG to first examine the occurrence and spatial distribution of these three EEG features in healthy infants and second to evaluate a predictive relationship with later behavioral outcomes. We report four key findings: First, infants’ EEG features appear locally: slow wave slope is maximal in occipital and frontal areas, whereas slow and fast spindle density is most pronounced frontocentrally. Second, slow waves and spindles are temporally coupled in infancy, with maximal coupling strength in the occipital areas of the brain. Third, slow wave slope, fast spindle density, and slow wave-spindle coupling are not associated with concurrent behavioral status (6 months). Fourth, fast spindle density in central and frontocentral regions at age 6 months predicts overall developmental status at age 12 months, and motor skills at age 12 and 24 months. Neither slow wave slope nor slow wave-spindle coupling predict later behavioral development. We further identified spindle frequency as a determinant of slow and fast spindle density, which accordingly, also predicts motor skills at 24 months. Our results propose fast spindle density, or alternatively spindle frequency, as early EEG biomarker for identifying thalamocortical maturation, which can potentially be used for early diagnosis of neurodevelopmental disorders in infants. These findings are in support of a role of sleep spindles in sensorimotor microcircuitry development. A crucial next step will be to evaluate whether early therapeutic interventions may be effective to reverse deviations in identified individuals at risk. |
| first_indexed | 2024-04-10T16:07:26Z |
| format | Article |
| id | doaj.art-b502e95852854a668e897478ae622a04 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-04-10T16:07:26Z |
| publishDate | 2023-04-01 |
| publisher | Elsevier |
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| series | NeuroImage |
| spelling | doaj.art-b502e95852854a668e897478ae622a042023-02-10T04:21:28ZengElsevierNeuroImage1095-95722023-04-01269119924An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancyValeria Jaramillo0Sarah F. Schoch1Andjela Markovic2Malcolm Kohler3Reto Huber4Caroline Lustenberger5Salome Kurth6Department of Pulmonology, University Hospital Zurich, Zurich, CH; Surrey Sleep Research Centre, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom; Neuromodulation Laboratory, School of Psychology, University of Surrey, Guildford, United KingdomDepartment of Pulmonology, University Hospital Zurich, Zurich, CH; Center of Competence Sleep & Health Zurich, University of Zurich, Zurich, CH; Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, NLDepartment of Pulmonology, University Hospital Zurich, Zurich, CH; Department of Psychology, University of Fribourg, Fribourg, CHDepartment of Pulmonology, University Hospital Zurich, Zurich, CH; Center of Competence Sleep & Health Zurich, University of Zurich, Zurich, CHChild Development Center, University Children's Hospital Zurich, Zurich, CH; Children's Research Center, University Children's Hospital Zurich, University of Zurich (UZH), Zürich, Switzerland; Center of Competence Sleep & Health Zurich, University of Zurich, Zurich, CH; Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, CHCenter of Competence Sleep & Health Zurich, University of Zurich, Zurich, CH; Neural Control of Movement Lab, Institute of Human Movement Sciences and Sport, Department of Health Sciences and Technology, ETH Zurich, 8092 Zurich, SwitzerlandDepartment of Pulmonology, University Hospital Zurich, Zurich, CH; Center of Competence Sleep & Health Zurich, University of Zurich, Zurich, CH; Department of Psychology, University of Fribourg, Fribourg, CH; Corresponding author at: Salome Kurth, University of Fribourg, Department of Psychology, Rue P.-A.-de-Faucigny 2, CH-1700 FribourgInfancy represents a critical period during which thalamocortical brain connections develop and mature. Deviations in the maturation of thalamocortical connectivity are linked to neurodevelopmental disorders. There is a lack of early biomarkers to detect and localize neuromaturational deviations, which can be overcome with mapping through high-density electroencephalography (hdEEG) assessed in sleep. Specifically, slow waves and spindles in non-rapid eye movement (NREM) sleep are generated by the thalamocortical system, and their characteristics, slow wave slope and spindle density, are closely related to neuroplasticity and learning. Spindles are often subdivided into slow (11.0-13.0 Hz) and fast (13.5-16.0 Hz) frequencies, for which not only different functions have been proposed, but for which also distinctive developmental trajectories have been reported across the first years of life. Recent studies further suggest that information processing during sleep underlying sleep-dependent learning is promoted by the temporal coupling of slow waves and spindles, yet slow wave-spindle coupling remains unexplored in infancy. Thus, we evaluated three potential biomarkers: 1) slow wave slope, 2) spindle density, and 3) the temporal coupling of slow waves with spindles. We use hdEEG to first examine the occurrence and spatial distribution of these three EEG features in healthy infants and second to evaluate a predictive relationship with later behavioral outcomes. We report four key findings: First, infants’ EEG features appear locally: slow wave slope is maximal in occipital and frontal areas, whereas slow and fast spindle density is most pronounced frontocentrally. Second, slow waves and spindles are temporally coupled in infancy, with maximal coupling strength in the occipital areas of the brain. Third, slow wave slope, fast spindle density, and slow wave-spindle coupling are not associated with concurrent behavioral status (6 months). Fourth, fast spindle density in central and frontocentral regions at age 6 months predicts overall developmental status at age 12 months, and motor skills at age 12 and 24 months. Neither slow wave slope nor slow wave-spindle coupling predict later behavioral development. We further identified spindle frequency as a determinant of slow and fast spindle density, which accordingly, also predicts motor skills at 24 months. Our results propose fast spindle density, or alternatively spindle frequency, as early EEG biomarker for identifying thalamocortical maturation, which can potentially be used for early diagnosis of neurodevelopmental disorders in infants. These findings are in support of a role of sleep spindles in sensorimotor microcircuitry development. A crucial next step will be to evaluate whether early therapeutic interventions may be effective to reverse deviations in identified individuals at risk.http://www.sciencedirect.com/science/article/pii/S1053811923000721High-density EEGDevelopmentInfancyBiomarkersThalamocortical connectivitySlow wave slope |
| spellingShingle | Valeria Jaramillo Sarah F. Schoch Andjela Markovic Malcolm Kohler Reto Huber Caroline Lustenberger Salome Kurth An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy NeuroImage High-density EEG Development Infancy Biomarkers Thalamocortical connectivity Slow wave slope |
| title | An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| title_full | An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| title_fullStr | An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| title_full_unstemmed | An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| title_short | An infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| title_sort | infant sleep electroencephalographic marker of thalamocortical connectivity predicts behavioral outcome in late infancy |
| topic | High-density EEG Development Infancy Biomarkers Thalamocortical connectivity Slow wave slope |
| url | http://www.sciencedirect.com/science/article/pii/S1053811923000721 |
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