Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task

Autores
Mininni, Camilo Juan; Zanutto, Bonifacio Silvano
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Animals are proposed to learn the latent rules governing their environment in order to maximize their chances of survival. However, rules may change without notice, forcing animals to keep a memory of which one is currently at work. Rule switching can lead to situations in which the same stimulus/response pairing is positively and negatively rewarded in the long run, depending on variables that are not accessible to the animal. This fact raises questions on how neural systems are capable of reinforcement learning in environments where the reinforcement is inconsistent. Here we address this issue by asking about which aspects of connectivity, neural excitability and synaptic plasticity are key for a very general, stochastic spiking neural network model to solve a task in which rules change without being cued, taking the serial reversal task (SRT) as paradigm. Contrary to what could be expected, we found strong limitations for biologically plausible networks to solve the SRT. Especially, we proved that no network of neurons can learn a SRT if it is a single neural population that integrates stimuli information and at the same time is responsible of choosing the behavioural response. This limitation is independent of the number of neurons, neuronal dynamics or plasticity rules, and arises from the fact that plasticity is locally computed at each synapse, and that synaptic changes and neuronal activity are mutually dependent processes. We propose and characterize a spiking neural network model that solves the SRT, which relies on separating the functions of stimuli integration and response selection. The model suggests that experimental efforts to understand neural function should focus on the characterization of neural circuits according to their connectivity, neural dynamics, and the degree of modulation of synaptic plasticity with reward.
Fil: Mininni, Camilo Juan. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Zanutto, Bonifacio Silvano. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; Argentina
Materia
SERIAL REVERSAL LEARNING
STABILITY-PLASTISITY DILEMMA
NEURAL NETWORK MODELS
THEORETICAL NEUROSCIENCE
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/41255

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spelling Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal taskMininni, Camilo JuanZanutto, Bonifacio SilvanoSERIAL REVERSAL LEARNINGSTABILITY-PLASTISITY DILEMMANEURAL NETWORK MODELSTHEORETICAL NEUROSCIENCEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Animals are proposed to learn the latent rules governing their environment in order to maximize their chances of survival. However, rules may change without notice, forcing animals to keep a memory of which one is currently at work. Rule switching can lead to situations in which the same stimulus/response pairing is positively and negatively rewarded in the long run, depending on variables that are not accessible to the animal. This fact raises questions on how neural systems are capable of reinforcement learning in environments where the reinforcement is inconsistent. Here we address this issue by asking about which aspects of connectivity, neural excitability and synaptic plasticity are key for a very general, stochastic spiking neural network model to solve a task in which rules change without being cued, taking the serial reversal task (SRT) as paradigm. Contrary to what could be expected, we found strong limitations for biologically plausible networks to solve the SRT. Especially, we proved that no network of neurons can learn a SRT if it is a single neural population that integrates stimuli information and at the same time is responsible of choosing the behavioural response. This limitation is independent of the number of neurons, neuronal dynamics or plasticity rules, and arises from the fact that plasticity is locally computed at each synapse, and that synaptic changes and neuronal activity are mutually dependent processes. We propose and characterize a spiking neural network model that solves the SRT, which relies on separating the functions of stimuli integration and response selection. The model suggests that experimental efforts to understand neural function should focus on the characterization of neural circuits according to their connectivity, neural dynamics, and the degree of modulation of synaptic plasticity with reward.Fil: Mininni, Camilo Juan. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Zanutto, Bonifacio Silvano. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; ArgentinaPublic Library of Science2017-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/41255Mininni, Camilo Juan; Zanutto, Bonifacio Silvano; Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task; Public Library of Science; Plos One; 12; 10; 10-2017; 1-26; e01869591932-6203CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0186959info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0186959info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-01-08T13:10:13Zoai:ri.conicet.gov.ar:11336/41255instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-01-08 13:10:13.95CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
title Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
spellingShingle Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
Mininni, Camilo Juan
SERIAL REVERSAL LEARNING
STABILITY-PLASTISITY DILEMMA
NEURAL NETWORK MODELS
THEORETICAL NEUROSCIENCE
title_short Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
title_full Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
title_fullStr Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
title_full_unstemmed Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
title_sort Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task
dc.creator.none.fl_str_mv Mininni, Camilo Juan
Zanutto, Bonifacio Silvano
author Mininni, Camilo Juan
author_facet Mininni, Camilo Juan
Zanutto, Bonifacio Silvano
author_role author
author2 Zanutto, Bonifacio Silvano
author2_role author
dc.subject.none.fl_str_mv SERIAL REVERSAL LEARNING
STABILITY-PLASTISITY DILEMMA
NEURAL NETWORK MODELS
THEORETICAL NEUROSCIENCE
topic SERIAL REVERSAL LEARNING
STABILITY-PLASTISITY DILEMMA
NEURAL NETWORK MODELS
THEORETICAL NEUROSCIENCE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Animals are proposed to learn the latent rules governing their environment in order to maximize their chances of survival. However, rules may change without notice, forcing animals to keep a memory of which one is currently at work. Rule switching can lead to situations in which the same stimulus/response pairing is positively and negatively rewarded in the long run, depending on variables that are not accessible to the animal. This fact raises questions on how neural systems are capable of reinforcement learning in environments where the reinforcement is inconsistent. Here we address this issue by asking about which aspects of connectivity, neural excitability and synaptic plasticity are key for a very general, stochastic spiking neural network model to solve a task in which rules change without being cued, taking the serial reversal task (SRT) as paradigm. Contrary to what could be expected, we found strong limitations for biologically plausible networks to solve the SRT. Especially, we proved that no network of neurons can learn a SRT if it is a single neural population that integrates stimuli information and at the same time is responsible of choosing the behavioural response. This limitation is independent of the number of neurons, neuronal dynamics or plasticity rules, and arises from the fact that plasticity is locally computed at each synapse, and that synaptic changes and neuronal activity are mutually dependent processes. We propose and characterize a spiking neural network model that solves the SRT, which relies on separating the functions of stimuli integration and response selection. The model suggests that experimental efforts to understand neural function should focus on the characterization of neural circuits according to their connectivity, neural dynamics, and the degree of modulation of synaptic plasticity with reward.
Fil: Mininni, Camilo Juan. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Zanutto, Bonifacio Silvano. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. Universidad de Buenos Aires. Facultad de Ingenieria. Instituto de Ingeniería Biomédica; Argentina
description Animals are proposed to learn the latent rules governing their environment in order to maximize their chances of survival. However, rules may change without notice, forcing animals to keep a memory of which one is currently at work. Rule switching can lead to situations in which the same stimulus/response pairing is positively and negatively rewarded in the long run, depending on variables that are not accessible to the animal. This fact raises questions on how neural systems are capable of reinforcement learning in environments where the reinforcement is inconsistent. Here we address this issue by asking about which aspects of connectivity, neural excitability and synaptic plasticity are key for a very general, stochastic spiking neural network model to solve a task in which rules change without being cued, taking the serial reversal task (SRT) as paradigm. Contrary to what could be expected, we found strong limitations for biologically plausible networks to solve the SRT. Especially, we proved that no network of neurons can learn a SRT if it is a single neural population that integrates stimuli information and at the same time is responsible of choosing the behavioural response. This limitation is independent of the number of neurons, neuronal dynamics or plasticity rules, and arises from the fact that plasticity is locally computed at each synapse, and that synaptic changes and neuronal activity are mutually dependent processes. We propose and characterize a spiking neural network model that solves the SRT, which relies on separating the functions of stimuli integration and response selection. The model suggests that experimental efforts to understand neural function should focus on the characterization of neural circuits according to their connectivity, neural dynamics, and the degree of modulation of synaptic plasticity with reward.
publishDate 2017
dc.date.none.fl_str_mv 2017-10
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/41255
Mininni, Camilo Juan; Zanutto, Bonifacio Silvano; Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task; Public Library of Science; Plos One; 12; 10; 10-2017; 1-26; e0186959
1932-6203
CONICET Digital
CONICET
url http://hdl.handle.net/11336/41255
identifier_str_mv Mininni, Camilo Juan; Zanutto, Bonifacio Silvano; Exploring the limits of learning: Segregation of information integration and response selection is required for learning a serial reversal task; Public Library of Science; Plos One; 12; 10; 10-2017; 1-26; e0186959
1932-6203
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0186959
info:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0186959
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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