Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex
Abstract Measures of functional connectivity have played a central role in advancing our understanding of how information is transmitted and processed within the brain. Traditionally, these studies have focused on identifying redundant functional connectivity, which involves determining when activit...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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SpringerOpen
2023-12-01
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| Series: | Brain Informatics |
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| Online Access: | https://doi.org/10.1186/s40708-023-00212-9 |
| _version_ | 1797397686165438464 |
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| author | Loren Koçillari Marco Celotto Nikolas A. Francis Shoutik Mukherjee Behtash Babadi Patrick O. Kanold Stefano Panzeri |
| author_facet | Loren Koçillari Marco Celotto Nikolas A. Francis Shoutik Mukherjee Behtash Babadi Patrick O. Kanold Stefano Panzeri |
| author_sort | Loren Koçillari |
| collection | DOAJ |
| description | Abstract Measures of functional connectivity have played a central role in advancing our understanding of how information is transmitted and processed within the brain. Traditionally, these studies have focused on identifying redundant functional connectivity, which involves determining when activity is similar across different sites or neurons. However, recent research has highlighted the importance of also identifying synergistic connectivity—that is, connectivity that gives rise to information not contained in either site or neuron alone. Here, we measured redundant and synergistic functional connectivity between neurons in the mouse primary auditory cortex during a sound discrimination task. Specifically, we measured directed functional connectivity between neurons simultaneously recorded with calcium imaging. We used Granger Causality as a functional connectivity measure. We then used Partial Information Decomposition to quantify the amount of redundant and synergistic information about the presented sound that is carried by functionally connected or functionally unconnected pairs of neurons. We found that functionally connected pairs present proportionally more redundant information and proportionally less synergistic information about sound than unconnected pairs, suggesting that their functional connectivity is primarily redundant. Further, synergy and redundancy coexisted both when mice made correct or incorrect perceptual discriminations. However, redundancy was much higher (both in absolute terms and in proportion to the total information available in neuron pairs) in correct behavioural choices compared to incorrect ones, whereas synergy was higher in absolute terms but lower in relative terms in correct than in incorrect behavioural choices. Moreover, the proportion of redundancy reliably predicted perceptual discriminations, with the proportion of synergy adding no extra predictive power. These results suggest a crucial contribution of redundancy to correct perceptual discriminations, possibly due to the advantage it offers for information propagation, and also suggest a role of synergy in enhancing information level during correct discriminations. |
| first_indexed | 2024-03-09T01:13:46Z |
| format | Article |
| id | doaj.art-8786b99c82074292bc2b9a5e9a4ae583 |
| institution | Directory Open Access Journal |
| issn | 2198-4018 2198-4026 |
| language | English |
| last_indexed | 2024-03-09T01:13:46Z |
| publishDate | 2023-12-01 |
| publisher | SpringerOpen |
| record_format | Article |
| series | Brain Informatics |
| spelling | doaj.art-8786b99c82074292bc2b9a5e9a4ae5832023-12-10T12:36:33ZengSpringerOpenBrain Informatics2198-40182198-40262023-12-0110111110.1186/s40708-023-00212-9Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortexLoren Koçillari0Marco Celotto1Nikolas A. Francis2Shoutik Mukherjee3Behtash Babadi4Patrick O. Kanold5Stefano Panzeri6Istituto Italiano Di TecnologiaIstituto Italiano Di TecnologiaDepartment of Biology and Brain and Behavior Institute, University of MarylandDepartment of Electrical and Computer Engineering and Institute for Systems Research, University of MarylandDepartment of Electrical and Computer Engineering and Institute for Systems Research, University of MarylandDepartment of Biomedical Engineering and Kavli Neuroscience Discovery Institute, Johns Hopkins UniversityDepartment of Excellence for Neural Information Processing, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf (UKE)Abstract Measures of functional connectivity have played a central role in advancing our understanding of how information is transmitted and processed within the brain. Traditionally, these studies have focused on identifying redundant functional connectivity, which involves determining when activity is similar across different sites or neurons. However, recent research has highlighted the importance of also identifying synergistic connectivity—that is, connectivity that gives rise to information not contained in either site or neuron alone. Here, we measured redundant and synergistic functional connectivity between neurons in the mouse primary auditory cortex during a sound discrimination task. Specifically, we measured directed functional connectivity between neurons simultaneously recorded with calcium imaging. We used Granger Causality as a functional connectivity measure. We then used Partial Information Decomposition to quantify the amount of redundant and synergistic information about the presented sound that is carried by functionally connected or functionally unconnected pairs of neurons. We found that functionally connected pairs present proportionally more redundant information and proportionally less synergistic information about sound than unconnected pairs, suggesting that their functional connectivity is primarily redundant. Further, synergy and redundancy coexisted both when mice made correct or incorrect perceptual discriminations. However, redundancy was much higher (both in absolute terms and in proportion to the total information available in neuron pairs) in correct behavioural choices compared to incorrect ones, whereas synergy was higher in absolute terms but lower in relative terms in correct than in incorrect behavioural choices. Moreover, the proportion of redundancy reliably predicted perceptual discriminations, with the proportion of synergy adding no extra predictive power. These results suggest a crucial contribution of redundancy to correct perceptual discriminations, possibly due to the advantage it offers for information propagation, and also suggest a role of synergy in enhancing information level during correct discriminations.https://doi.org/10.1186/s40708-023-00212-9Functional connectivityRedundancySynergyAuditory perception |
| spellingShingle | Loren Koçillari Marco Celotto Nikolas A. Francis Shoutik Mukherjee Behtash Babadi Patrick O. Kanold Stefano Panzeri Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex Brain Informatics Functional connectivity Redundancy Synergy Auditory perception |
| title | Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| title_full | Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| title_fullStr | Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| title_full_unstemmed | Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| title_short | Behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| title_sort | behavioural relevance of redundant and synergistic stimulus information between functionally connected neurons in mouse auditory cortex |
| topic | Functional connectivity Redundancy Synergy Auditory perception |
| url | https://doi.org/10.1186/s40708-023-00212-9 |
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