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Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits

Sleep spindles are associated with the beginning of deep sleep and memory consolidation and are disrupted in schizophrenia and autism. In primates, distinct core and matrix thalamocortical (TC) circuits regulate sleep spindle activity through communications that are filtered by the inhibitory thalam...

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Autores principales: Yazdanbakhsh, Arash, Barbas, Helen, Zikopoulos, Basilis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312265/
https://www.ncbi.nlm.nih.gov/pubmed/37397882
http://dx.doi.org/10.1162/netn_a_00311
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author Yazdanbakhsh, Arash
Barbas, Helen
Zikopoulos, Basilis
author_facet Yazdanbakhsh, Arash
Barbas, Helen
Zikopoulos, Basilis
author_sort Yazdanbakhsh, Arash
collection PubMed
description Sleep spindles are associated with the beginning of deep sleep and memory consolidation and are disrupted in schizophrenia and autism. In primates, distinct core and matrix thalamocortical (TC) circuits regulate sleep spindle activity through communications that are filtered by the inhibitory thalamic reticular nucleus (TRN); however, little is known about typical TC network interactions and the mechanisms that are disrupted in brain disorders. We developed a primate-specific, circuit-based TC computational model with distinct core and matrix loops that can simulate sleep spindles. We implemented novel multilevel cortical and thalamic mixing, and included local thalamic inhibitory interneurons, and direct layer 5 projections of variable density to TRN and thalamus to investigate the functional consequences of different ratios of core and matrix node connectivity contribution to spindle dynamics. Our simulations showed that spindle power in primates can be modulated based on the level of cortical feedback, thalamic inhibition, and engagement of model core versus matrix, with the latter having a greater role in spindle dynamics. The study of the distinct spatial and temporal dynamics of core-, matrix-, and mix-generated sleep spindles establishes a framework to study disruption of TC circuit balance underlying deficits in sleep and attentional gating seen in autism and schizophrenia.
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spelling pubmed-103122652023-07-01 Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits Yazdanbakhsh, Arash Barbas, Helen Zikopoulos, Basilis Netw Neurosci Research Article Sleep spindles are associated with the beginning of deep sleep and memory consolidation and are disrupted in schizophrenia and autism. In primates, distinct core and matrix thalamocortical (TC) circuits regulate sleep spindle activity through communications that are filtered by the inhibitory thalamic reticular nucleus (TRN); however, little is known about typical TC network interactions and the mechanisms that are disrupted in brain disorders. We developed a primate-specific, circuit-based TC computational model with distinct core and matrix loops that can simulate sleep spindles. We implemented novel multilevel cortical and thalamic mixing, and included local thalamic inhibitory interneurons, and direct layer 5 projections of variable density to TRN and thalamus to investigate the functional consequences of different ratios of core and matrix node connectivity contribution to spindle dynamics. Our simulations showed that spindle power in primates can be modulated based on the level of cortical feedback, thalamic inhibition, and engagement of model core versus matrix, with the latter having a greater role in spindle dynamics. The study of the distinct spatial and temporal dynamics of core-, matrix-, and mix-generated sleep spindles establishes a framework to study disruption of TC circuit balance underlying deficits in sleep and attentional gating seen in autism and schizophrenia. MIT Press 2023-06-30 /pmc/articles/PMC10312265/ /pubmed/37397882 http://dx.doi.org/10.1162/netn_a_00311 Text en © 2023 Massachusetts Institute of Technology https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. For a full description of the license, please visit https://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Yazdanbakhsh, Arash
Barbas, Helen
Zikopoulos, Basilis
Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title_full Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title_fullStr Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title_full_unstemmed Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title_short Sleep spindles in primates: Modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
title_sort sleep spindles in primates: modeling the effects of distinct laminar thalamocortical connectivity in core, matrix, and reticular thalamic circuits
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312265/
https://www.ncbi.nlm.nih.gov/pubmed/37397882
http://dx.doi.org/10.1162/netn_a_00311
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