Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.

In rodent visual cortex, synaptic connections between orientation-selective neurons are unspecific at the time of eye opening, and become to some degree functionally specific only later during development. An explanation for this two-stage process was proposed in terms of Hebbian plasticity based on...

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Main Authors: Sadra Sadeh, Claudia Clopath, Stefan Rotter
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-06-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4474917?pdf=render
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spelling doaj-0d2cb1fefe4240b590671ea806ea246c2020-11-25T01:32:26ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-06-01116e100430710.1371/journal.pcbi.1004307Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.Sadra SadehClaudia ClopathStefan RotterIn rodent visual cortex, synaptic connections between orientation-selective neurons are unspecific at the time of eye opening, and become to some degree functionally specific only later during development. An explanation for this two-stage process was proposed in terms of Hebbian plasticity based on visual experience that would eventually enhance connections between neurons with similar response features. For this to work, however, two conditions must be satisfied: First, orientation selective neuronal responses must exist before specific recurrent synaptic connections can be established. Second, Hebbian learning must be compatible with the recurrent network dynamics contributing to orientation selectivity, and the resulting specific connectivity must remain stable for unspecific background activity. Previous studies have mainly focused on very simple models, where the receptive fields of neurons were essentially determined by feedforward mechanisms, and where the recurrent network was small, lacking the complex recurrent dynamics of large-scale networks of excitatory and inhibitory neurons. Here we studied the emergence of functionally specific connectivity in large-scale recurrent networks with synaptic plasticity. Our results show that balanced random networks, which already exhibit highly selective responses at eye opening, can develop feature-specific connectivity if appropriate rules of synaptic plasticity are invoked within and between excitatory and inhibitory populations. If these conditions are met, the initial orientation selectivity guides the process of Hebbian learning and, as a result, functionally specific and a surplus of bidirectional connections emerge. Our results thus demonstrate the cooperation of synaptic plasticity and recurrent dynamics in large-scale functional networks with realistic receptive fields, highlight the role of inhibition as a critical element in this process, and paves the road for further computational studies of sensory processing in neocortical network models equipped with synaptic plasticity.http://europepmc.org/articles/PMC4474917?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sadra Sadeh
Claudia Clopath
Stefan Rotter
spellingShingle Sadra Sadeh
Claudia Clopath
Stefan Rotter
Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
PLoS Computational Biology
author_facet Sadra Sadeh
Claudia Clopath
Stefan Rotter
author_sort Sadra Sadeh
title Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
title_short Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
title_full Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
title_fullStr Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
title_full_unstemmed Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity.
title_sort emergence of functional specificity in balanced networks with synaptic plasticity.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2015-06-01
description In rodent visual cortex, synaptic connections between orientation-selective neurons are unspecific at the time of eye opening, and become to some degree functionally specific only later during development. An explanation for this two-stage process was proposed in terms of Hebbian plasticity based on visual experience that would eventually enhance connections between neurons with similar response features. For this to work, however, two conditions must be satisfied: First, orientation selective neuronal responses must exist before specific recurrent synaptic connections can be established. Second, Hebbian learning must be compatible with the recurrent network dynamics contributing to orientation selectivity, and the resulting specific connectivity must remain stable for unspecific background activity. Previous studies have mainly focused on very simple models, where the receptive fields of neurons were essentially determined by feedforward mechanisms, and where the recurrent network was small, lacking the complex recurrent dynamics of large-scale networks of excitatory and inhibitory neurons. Here we studied the emergence of functionally specific connectivity in large-scale recurrent networks with synaptic plasticity. Our results show that balanced random networks, which already exhibit highly selective responses at eye opening, can develop feature-specific connectivity if appropriate rules of synaptic plasticity are invoked within and between excitatory and inhibitory populations. If these conditions are met, the initial orientation selectivity guides the process of Hebbian learning and, as a result, functionally specific and a surplus of bidirectional connections emerge. Our results thus demonstrate the cooperation of synaptic plasticity and recurrent dynamics in large-scale functional networks with realistic receptive fields, highlight the role of inhibition as a critical element in this process, and paves the road for further computational studies of sensory processing in neocortical network models equipped with synaptic plasticity.
url http://europepmc.org/articles/PMC4474917?pdf=render
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