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Laminar dynamics of high amplitude beta bursts in human motor cortex

Motor cortical activity in the beta frequency range is one of the strongest and most studied movement-related neural signals. At the single trial level, beta band activity is often characterized by transient, high amplitude, bursting events rather than slowly modulating oscillations. The timing of t...

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Autores principales: Bonaiuto, James J, Little, Simon, Neymotin, Samuel A, Jones, Stephanie R, Barnes, Gareth R, Bestmann, Sven
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8463839/
https://www.ncbi.nlm.nih.gov/pubmed/34407440
http://dx.doi.org/10.1016/j.neuroimage.2021.118479
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author Bonaiuto, James J
Little, Simon
Neymotin, Samuel A
Jones, Stephanie R
Barnes, Gareth R
Bestmann, Sven
author_facet Bonaiuto, James J
Little, Simon
Neymotin, Samuel A
Jones, Stephanie R
Barnes, Gareth R
Bestmann, Sven
author_sort Bonaiuto, James J
collection PubMed
description Motor cortical activity in the beta frequency range is one of the strongest and most studied movement-related neural signals. At the single trial level, beta band activity is often characterized by transient, high amplitude, bursting events rather than slowly modulating oscillations. The timing of these bursting events is tightly linked to behavior, suggesting a more dynamic functional role for beta activity than previously believed. However, the neural mechanisms underlying beta bursts in sensorimotor circuits are poorly understood. To address this, we here leverage and extend recent developments in high precision MEG for temporally resolved laminar analysis of burst activity, combined with a neocortical circuit model that simulates the biophysical generators of the electrical currents which drive beta bursts. This approach pinpoints the generation of beta bursts in human motor cortex to distinct excitatory synaptic inputs to deep and superficial cortical layers, which drive current flow in opposite directions. These laminar dynamics of beta bursts in motor cortex align with prior invasive animal recordings within the somatosensory cortex, and suggest a conserved mechanism for somatosensory and motor cortical beta bursts. More generally, we demonstrate the ability for uncovering the laminar dynamics of event-related neural signals in human non-invasive recordings. This provides important constraints to theories about the functional role of burst activity for movement control in health and disease, and crucial links between macro-scale phenomena measured in humans and micro-circuit activity recorded from animal models.
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spelling pubmed-84638392021-11-15 Laminar dynamics of high amplitude beta bursts in human motor cortex Bonaiuto, James J Little, Simon Neymotin, Samuel A Jones, Stephanie R Barnes, Gareth R Bestmann, Sven Neuroimage Article Motor cortical activity in the beta frequency range is one of the strongest and most studied movement-related neural signals. At the single trial level, beta band activity is often characterized by transient, high amplitude, bursting events rather than slowly modulating oscillations. The timing of these bursting events is tightly linked to behavior, suggesting a more dynamic functional role for beta activity than previously believed. However, the neural mechanisms underlying beta bursts in sensorimotor circuits are poorly understood. To address this, we here leverage and extend recent developments in high precision MEG for temporally resolved laminar analysis of burst activity, combined with a neocortical circuit model that simulates the biophysical generators of the electrical currents which drive beta bursts. This approach pinpoints the generation of beta bursts in human motor cortex to distinct excitatory synaptic inputs to deep and superficial cortical layers, which drive current flow in opposite directions. These laminar dynamics of beta bursts in motor cortex align with prior invasive animal recordings within the somatosensory cortex, and suggest a conserved mechanism for somatosensory and motor cortical beta bursts. More generally, we demonstrate the ability for uncovering the laminar dynamics of event-related neural signals in human non-invasive recordings. This provides important constraints to theories about the functional role of burst activity for movement control in health and disease, and crucial links between macro-scale phenomena measured in humans and micro-circuit activity recorded from animal models. Academic Press 2021-11-15 /pmc/articles/PMC8463839/ /pubmed/34407440 http://dx.doi.org/10.1016/j.neuroimage.2021.118479 Text en © 2021 The Authors. Published by Elsevier Inc. https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bonaiuto, James J
Little, Simon
Neymotin, Samuel A
Jones, Stephanie R
Barnes, Gareth R
Bestmann, Sven
Laminar dynamics of high amplitude beta bursts in human motor cortex
title Laminar dynamics of high amplitude beta bursts in human motor cortex
title_full Laminar dynamics of high amplitude beta bursts in human motor cortex
title_fullStr Laminar dynamics of high amplitude beta bursts in human motor cortex
title_full_unstemmed Laminar dynamics of high amplitude beta bursts in human motor cortex
title_short Laminar dynamics of high amplitude beta bursts in human motor cortex
title_sort laminar dynamics of high amplitude beta bursts in human motor cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8463839/
https://www.ncbi.nlm.nih.gov/pubmed/34407440
http://dx.doi.org/10.1016/j.neuroimage.2021.118479
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