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Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning

Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuron...

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Detalles Bibliográficos
Autores principales: Gillett, Maxwell, Pereira, Ulises, Brunel, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703604/
https://www.ncbi.nlm.nih.gov/pubmed/33177232
http://dx.doi.org/10.1073/pnas.1918674117
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author Gillett, Maxwell
Pereira, Ulises
Brunel, Nicolas
author_facet Gillett, Maxwell
Pereira, Ulises
Brunel, Nicolas
author_sort Gillett, Maxwell
collection PubMed
description Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations.
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spelling pubmed-77036042020-12-10 Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning Gillett, Maxwell Pereira, Ulises Brunel, Nicolas Proc Natl Acad Sci U S A Biological Sciences Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations. National Academy of Sciences 2020-11-24 2020-11-11 /pmc/articles/PMC7703604/ /pubmed/33177232 http://dx.doi.org/10.1073/pnas.1918674117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Gillett, Maxwell
Pereira, Ulises
Brunel, Nicolas
Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title_full Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title_fullStr Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title_full_unstemmed Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title_short Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning
title_sort characteristics of sequential activity in networks with temporally asymmetric hebbian learning
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703604/
https://www.ncbi.nlm.nih.gov/pubmed/33177232
http://dx.doi.org/10.1073/pnas.1918674117
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