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State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics

This work studies the evolution of cortical networks during the transition from escape strategy to avoidance strategy in auditory discrimination learning in Mongolian gerbils trained by the well-established two-way active avoidance learning paradigm. The animals were implanted with electrode arrays...

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Autores principales: Kozma, Robert, Hu, Sanqing, Sokolov, Yury, Wanger, Tim, Schulz, Andreas L., Woldeit, Marie L., Gonçalves, Ana I., Ruszinkó, Miklós, Ohl, Frank W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8100519/
https://www.ncbi.nlm.nih.gov/pubmed/33967706
http://dx.doi.org/10.3389/fnsys.2021.641684
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author Kozma, Robert
Hu, Sanqing
Sokolov, Yury
Wanger, Tim
Schulz, Andreas L.
Woldeit, Marie L.
Gonçalves, Ana I.
Ruszinkó, Miklós
Ohl, Frank W.
author_facet Kozma, Robert
Hu, Sanqing
Sokolov, Yury
Wanger, Tim
Schulz, Andreas L.
Woldeit, Marie L.
Gonçalves, Ana I.
Ruszinkó, Miklós
Ohl, Frank W.
author_sort Kozma, Robert
collection PubMed
description This work studies the evolution of cortical networks during the transition from escape strategy to avoidance strategy in auditory discrimination learning in Mongolian gerbils trained by the well-established two-way active avoidance learning paradigm. The animals were implanted with electrode arrays centered on the surface of the primary auditory cortex and electrocorticogram (ECoG) recordings were made during performance of an auditory Go/NoGo discrimination task. Our experiments confirm previous results on a sudden behavioral change from the initial naïve state to an avoidance strategy as learning progresses. We employed two causality metrics using Granger Causality (GC) and New Causality (NC) to quantify changes in the causality flow between ECoG channels as the animals switched to avoidance strategy. We found that the number of channel pairs with inverse causal interaction significantly increased after the animal acquired successful discrimination, which indicates structural changes in the cortical networks as a result of learning. A suitable graph-theoretical model is developed to interpret the findings in terms of cortical networks evolving during cognitive state transitions. Structural changes lead to changes in the dynamics of neural populations, which are described as phase transitions in the network graph model with small-world connections. Overall, our findings underscore the importance of functional reorganization in sensory cortical areas as a possible neural contributor to behavioral changes.
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spelling pubmed-81005192021-05-07 State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics Kozma, Robert Hu, Sanqing Sokolov, Yury Wanger, Tim Schulz, Andreas L. Woldeit, Marie L. Gonçalves, Ana I. Ruszinkó, Miklós Ohl, Frank W. Front Syst Neurosci Neuroscience This work studies the evolution of cortical networks during the transition from escape strategy to avoidance strategy in auditory discrimination learning in Mongolian gerbils trained by the well-established two-way active avoidance learning paradigm. The animals were implanted with electrode arrays centered on the surface of the primary auditory cortex and electrocorticogram (ECoG) recordings were made during performance of an auditory Go/NoGo discrimination task. Our experiments confirm previous results on a sudden behavioral change from the initial naïve state to an avoidance strategy as learning progresses. We employed two causality metrics using Granger Causality (GC) and New Causality (NC) to quantify changes in the causality flow between ECoG channels as the animals switched to avoidance strategy. We found that the number of channel pairs with inverse causal interaction significantly increased after the animal acquired successful discrimination, which indicates structural changes in the cortical networks as a result of learning. A suitable graph-theoretical model is developed to interpret the findings in terms of cortical networks evolving during cognitive state transitions. Structural changes lead to changes in the dynamics of neural populations, which are described as phase transitions in the network graph model with small-world connections. Overall, our findings underscore the importance of functional reorganization in sensory cortical areas as a possible neural contributor to behavioral changes. Frontiers Media S.A. 2021-04-22 /pmc/articles/PMC8100519/ /pubmed/33967706 http://dx.doi.org/10.3389/fnsys.2021.641684 Text en Copyright © 2021 Kozma, Hu, Sokolov, Wanger, Schulz, Woldeit, Gonçalves, Ruszinkó and Ohl. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Kozma, Robert
Hu, Sanqing
Sokolov, Yury
Wanger, Tim
Schulz, Andreas L.
Woldeit, Marie L.
Gonçalves, Ana I.
Ruszinkó, Miklós
Ohl, Frank W.
State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title_full State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title_fullStr State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title_full_unstemmed State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title_short State Transitions During Discrimination Learning in the Gerbil Auditory Cortex Analyzed by Network Causality Metrics
title_sort state transitions during discrimination learning in the gerbil auditory cortex analyzed by network causality metrics
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8100519/
https://www.ncbi.nlm.nih.gov/pubmed/33967706
http://dx.doi.org/10.3389/fnsys.2021.641684
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