Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales

AbstractNeural information processing is widely understood to depend on correlations in neuronal activity. However, whether correlation is favorable or not is contentious. Here, we sought to determine how correlated activity and information processing are related in cortical circuits. Using recordin...

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Main Authors: Samantha P. Sherrill, Nicholas M. Timme, John M. Beggs, Ehren L. Newman
Format: Article
Language:English
Published: The MIT Press 2020-07-01
Series:Network Neuroscience
Online Access:https://direct.mit.edu/netn/article/4/3/678/95833/Correlated-activity-favors-synergistic-processing
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author Samantha P. Sherrill
Nicholas M. Timme
John M. Beggs
Ehren L. Newman
author_facet Samantha P. Sherrill
Nicholas M. Timme
John M. Beggs
Ehren L. Newman
author_sort Samantha P. Sherrill
collection DOAJ
description AbstractNeural information processing is widely understood to depend on correlations in neuronal activity. However, whether correlation is favorable or not is contentious. Here, we sought to determine how correlated activity and information processing are related in cortical circuits. Using recordings of hundreds of spiking neurons in organotypic cultures of mouse neocortex, we asked whether mutual information between neurons that feed into a common third neuron increased synergistic information processing by the receiving neuron. We found that mutual information and synergistic processing were positively related at synaptic timescales (0.05–14 ms), where mutual information values were low. This effect was mediated by the increase in information transmission—of which synergistic processing is a component—that resulted as mutual information grew. However, at extrasynaptic windows (up to 3,000 ms), where mutual information values were high, the relationship between mutual information and synergistic processing became negative. In this regime, greater mutual information resulted in a disproportionate increase in redundancy relative to information transmission. These results indicate that the emergence of synergistic processing from correlated activity differs according to timescale and correlation regime. In a low-correlation regime, synergistic processing increases with greater correlation, and in a high-correlation regime, synergistic processing decreases with greater correlation.
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spelling doaj.art-3bbf8b9731b74357b4c217bb4094de212022-12-21T23:59:05ZengThe MIT PressNetwork Neuroscience2472-17512020-07-014367869710.1162/netn_a_00141Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescalesSamantha P. Sherrill0http://orcid.org/0000-0002-2894-7138Nicholas M. Timme1John M. Beggs2Ehren L. Newman3Department of Psychological and Brain Sciences and Program in Neuroscience, Indiana University Bloomington, Bloomington, IN, USADepartment of Psychology, Indiana University-Purdue University Indianapolis, Indianapolis, IN, USADepartment of Physics & Program in Neuroscience, Indiana University Bloomington, Bloomington, IN, USADepartment of Psychological and Brain Sciences and Program in Neuroscience, Indiana University Bloomington, Bloomington, IN, USAAbstractNeural information processing is widely understood to depend on correlations in neuronal activity. However, whether correlation is favorable or not is contentious. Here, we sought to determine how correlated activity and information processing are related in cortical circuits. Using recordings of hundreds of spiking neurons in organotypic cultures of mouse neocortex, we asked whether mutual information between neurons that feed into a common third neuron increased synergistic information processing by the receiving neuron. We found that mutual information and synergistic processing were positively related at synaptic timescales (0.05–14 ms), where mutual information values were low. This effect was mediated by the increase in information transmission—of which synergistic processing is a component—that resulted as mutual information grew. However, at extrasynaptic windows (up to 3,000 ms), where mutual information values were high, the relationship between mutual information and synergistic processing became negative. In this regime, greater mutual information resulted in a disproportionate increase in redundancy relative to information transmission. These results indicate that the emergence of synergistic processing from correlated activity differs according to timescale and correlation regime. In a low-correlation regime, synergistic processing increases with greater correlation, and in a high-correlation regime, synergistic processing decreases with greater correlation.https://direct.mit.edu/netn/article/4/3/678/95833/Correlated-activity-favors-synergistic-processing
spellingShingle Samantha P. Sherrill
Nicholas M. Timme
John M. Beggs
Ehren L. Newman
Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
Network Neuroscience
title Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
title_full Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
title_fullStr Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
title_full_unstemmed Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
title_short Correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
title_sort correlated activity favors synergistic processing in local cortical networks in vitro at synaptically relevant timescales
url https://direct.mit.edu/netn/article/4/3/678/95833/Correlated-activity-favors-synergistic-processing
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AT johnmbeggs correlatedactivityfavorssynergisticprocessinginlocalcorticalnetworksinvitroatsynapticallyrelevanttimescales
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