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Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition

Stereotyped sequences of neural activity are thought to underlie reproducible behaviors and cognitive processes ranging from memory recall to arm movement. One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activit...

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Detalles Bibliográficos
Autores principales: Cannon, Jonathan, Kopell, Nancy, Gardner, Timothy, Markowitz, Jeffrey
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633124/
https://www.ncbi.nlm.nih.gov/pubmed/26536029
http://dx.doi.org/10.1371/journal.pcbi.1004581
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author Cannon, Jonathan
Kopell, Nancy
Gardner, Timothy
Markowitz, Jeffrey
author_facet Cannon, Jonathan
Kopell, Nancy
Gardner, Timothy
Markowitz, Jeffrey
author_sort Cannon, Jonathan
collection PubMed
description Stereotyped sequences of neural activity are thought to underlie reproducible behaviors and cognitive processes ranging from memory recall to arm movement. One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation. But recent experimental observations in the avian song production pathway during song generation have shown excitatory activity interacting strongly with the firing patterns of inhibitory neurons, suggesting a process of sequence generation more complex than feedforward excitation. Here we propose a model of sequence generation inspired by these observations in which a pulse travels along a spatially recurrent excitatory chain, passing repeatedly through zones of local feedback inhibition. In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network. These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation.
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spelling pubmed-46331242015-11-13 Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition Cannon, Jonathan Kopell, Nancy Gardner, Timothy Markowitz, Jeffrey PLoS Comput Biol Research Article Stereotyped sequences of neural activity are thought to underlie reproducible behaviors and cognitive processes ranging from memory recall to arm movement. One of the most prominent theoretical models of neural sequence generation is the synfire chain, in which pulses of synchronized spiking activity propagate robustly along a chain of cells connected by highly redundant feedforward excitation. But recent experimental observations in the avian song production pathway during song generation have shown excitatory activity interacting strongly with the firing patterns of inhibitory neurons, suggesting a process of sequence generation more complex than feedforward excitation. Here we propose a model of sequence generation inspired by these observations in which a pulse travels along a spatially recurrent excitatory chain, passing repeatedly through zones of local feedback inhibition. In this model, synchrony and robust timing are maintained not through redundant excitatory connections, but rather through the interaction between the pulse and the spatiotemporal pattern of inhibition that it creates as it circulates the network. These results suggest that spatially and temporally structured inhibition may play a key role in sequence generation. Public Library of Science 2015-11-04 /pmc/articles/PMC4633124/ /pubmed/26536029 http://dx.doi.org/10.1371/journal.pcbi.1004581 Text en © 2015 Cannon et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Cannon, Jonathan
Kopell, Nancy
Gardner, Timothy
Markowitz, Jeffrey
Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title_full Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title_fullStr Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title_full_unstemmed Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title_short Neural Sequence Generation Using Spatiotemporal Patterns of Inhibition
title_sort neural sequence generation using spatiotemporal patterns of inhibition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633124/
https://www.ncbi.nlm.nih.gov/pubmed/26536029
http://dx.doi.org/10.1371/journal.pcbi.1004581
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AT markowitzjeffrey neuralsequencegenerationusingspatiotemporalpatternsofinhibition