Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.

Synchronous oscillations in neural populations are considered being controlled by inhibitory neurons. In the granular layer of the cerebellum, two major types of cells are excitatory granular cells (GCs) and inhibitory Golgi cells (GoCs). GC spatiotemporal dynamics, as the output of the granular lay...

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Autores principales: Yuanhong Tang, Lingling An, Quan Wang, Jian K Liu
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:e61bf90f851542a48462d0714cb612562021-11-25T05:40:34ZRegulating synchronous oscillations of cerebellar granule cells by different types of inhibition.1553-734X1553-735810.1371/journal.pcbi.1009163https://doaj.org/article/e61bf90f851542a48462d0714cb612562021-06-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009163https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Synchronous oscillations in neural populations are considered being controlled by inhibitory neurons. In the granular layer of the cerebellum, two major types of cells are excitatory granular cells (GCs) and inhibitory Golgi cells (GoCs). GC spatiotemporal dynamics, as the output of the granular layer, is highly regulated by GoCs. However, there are various types of inhibition implemented by GoCs. With inputs from mossy fibers, GCs and GoCs are reciprocally connected to exhibit different network motifs of synaptic connections. From the view of GCs, feedforward inhibition is expressed as the direct input from GoCs excited by mossy fibers, whereas feedback inhibition is from GoCs via GCs themselves. In addition, there are abundant gap junctions between GoCs showing another form of inhibition. It remains unclear how these diverse copies of inhibition regulate neural population oscillation changes. Leveraging a computational model of the granular layer network, we addressed this question to examine the emergence and modulation of network oscillation using different types of inhibition. We show that at the network level, feedback inhibition is crucial to generate neural oscillation. When short-term plasticity was equipped on GoC-GC synapses, oscillations were largely diminished. Robust oscillations can only appear with additional gap junctions. Moreover, there was a substantial level of cross-frequency coupling in oscillation dynamics. Such a coupling was adjusted and strengthened by GoCs through feedback inhibition. Taken together, our results suggest that the cooperation of distinct types of GoC inhibition plays an essential role in regulating synchronous oscillations of the GC population. With GCs as the sole output of the granular network, their oscillation dynamics could potentially enhance the computational capability of downstream neurons.Yuanhong TangLingling AnQuan WangJian K LiuPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 6, p e1009163 (2021)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Yuanhong Tang
Lingling An
Quan Wang
Jian K Liu
Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
description Synchronous oscillations in neural populations are considered being controlled by inhibitory neurons. In the granular layer of the cerebellum, two major types of cells are excitatory granular cells (GCs) and inhibitory Golgi cells (GoCs). GC spatiotemporal dynamics, as the output of the granular layer, is highly regulated by GoCs. However, there are various types of inhibition implemented by GoCs. With inputs from mossy fibers, GCs and GoCs are reciprocally connected to exhibit different network motifs of synaptic connections. From the view of GCs, feedforward inhibition is expressed as the direct input from GoCs excited by mossy fibers, whereas feedback inhibition is from GoCs via GCs themselves. In addition, there are abundant gap junctions between GoCs showing another form of inhibition. It remains unclear how these diverse copies of inhibition regulate neural population oscillation changes. Leveraging a computational model of the granular layer network, we addressed this question to examine the emergence and modulation of network oscillation using different types of inhibition. We show that at the network level, feedback inhibition is crucial to generate neural oscillation. When short-term plasticity was equipped on GoC-GC synapses, oscillations were largely diminished. Robust oscillations can only appear with additional gap junctions. Moreover, there was a substantial level of cross-frequency coupling in oscillation dynamics. Such a coupling was adjusted and strengthened by GoCs through feedback inhibition. Taken together, our results suggest that the cooperation of distinct types of GoC inhibition plays an essential role in regulating synchronous oscillations of the GC population. With GCs as the sole output of the granular network, their oscillation dynamics could potentially enhance the computational capability of downstream neurons.
format article
author Yuanhong Tang
Lingling An
Quan Wang
Jian K Liu
author_facet Yuanhong Tang
Lingling An
Quan Wang
Jian K Liu
author_sort Yuanhong Tang
title Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
title_short Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
title_full Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
title_fullStr Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
title_full_unstemmed Regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
title_sort regulating synchronous oscillations of cerebellar granule cells by different types of inhibition.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/e61bf90f851542a48462d0714cb61256
work_keys_str_mv AT yuanhongtang regulatingsynchronousoscillationsofcerebellargranulecellsbydifferenttypesofinhibition
AT linglingan regulatingsynchronousoscillationsofcerebellargranulecellsbydifferenttypesofinhibition
AT quanwang regulatingsynchronousoscillationsofcerebellargranulecellsbydifferenttypesofinhibition
AT jiankliu regulatingsynchronousoscillationsofcerebellargranulecellsbydifferenttypesofinhibition
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