A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields
Summary: Hippocampus place cell discharge is temporally unreliable across seconds and days, and place fields are multimodal, suggesting an “ensemble cofiring” spatial coding hypothesis with manifold dynamics that does not require reliable spatial tuning, in contrast to hypotheses based on place fiel...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723011543 |
| _version_ | 1797676280921980928 |
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| author | Eliott Robert Joseph Levy Simón Carrillo-Segura Eun Hye Park William Thomas Redman José Rafael Hurtado SueYeon Chung André Antonio Fenton |
| author_facet | Eliott Robert Joseph Levy Simón Carrillo-Segura Eun Hye Park William Thomas Redman José Rafael Hurtado SueYeon Chung André Antonio Fenton |
| author_sort | Eliott Robert Joseph Levy |
| collection | DOAJ |
| description | Summary: Hippocampus place cell discharge is temporally unreliable across seconds and days, and place fields are multimodal, suggesting an “ensemble cofiring” spatial coding hypothesis with manifold dynamics that does not require reliable spatial tuning, in contrast to hypotheses based on place field (spatial tuning) stability. We imaged mouse CA1 (cornu ammonis 1) ensembles in two environments across three weeks to evaluate these coding hypotheses. While place fields “remap,” being more distinct between than within environments, coactivity relationships generally change less. Decoding location and environment from 1-s ensemble location-specific activity is effective and improves with experience. Decoding environment from cell-pair coactivity relationships is also effective and improves with experience, even after removing place tuning. Discriminating environments from 1-s ensemble coactivity relies crucially on the cells with the most anti-coactive cell-pair relationships because activity is internally organized on a low-dimensional manifold of non-linear coactivity relationships that intermittently reregisters to environments according to the anti-cofiring subpopulation activity. |
| first_indexed | 2024-03-11T22:26:42Z |
| format | Article |
| id | doaj.art-43eb060bbeae4a7f9060f1161bf86ad5 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-11T22:26:42Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-43eb060bbeae4a7f9060f1161bf86ad52023-09-24T05:15:02ZengElsevierCell Reports2211-12472023-10-014210113142A manifold neural population code for space in hippocampal coactivity dynamics independent of place fieldsEliott Robert Joseph Levy0Simón Carrillo-Segura1Eun Hye Park2William Thomas Redman3José Rafael Hurtado4SueYeon Chung5André Antonio Fenton6Center for Neural Science, New York University, New York, NY 10003, USACenter for Neural Science, New York University, New York, NY 10003, USA; Graduate Program in Mechanical and Aerospace Engineering, Tandon School of Engineering, New York University, Brooklyn, NY 11201, USACenter for Neural Science, New York University, New York, NY 10003, USAInterdepartmental Graduate Program in Dynamical Neuroscience, University of California, Santa Barbara, Santa Barbara, CA 93106, USACenter for Neural Science, New York University, New York, NY 10003, USACenter for Neural Science, New York University, New York, NY 10003, USA; Flatiron Institute Center for Computational Neuroscience, New York, NY 10010, USACenter for Neural Science, New York University, New York, NY 10003, USA; Neuroscience Institute at the NYU Langone Medical Center, New York, NY 10016, USA; Corresponding authorSummary: Hippocampus place cell discharge is temporally unreliable across seconds and days, and place fields are multimodal, suggesting an “ensemble cofiring” spatial coding hypothesis with manifold dynamics that does not require reliable spatial tuning, in contrast to hypotheses based on place field (spatial tuning) stability. We imaged mouse CA1 (cornu ammonis 1) ensembles in two environments across three weeks to evaluate these coding hypotheses. While place fields “remap,” being more distinct between than within environments, coactivity relationships generally change less. Decoding location and environment from 1-s ensemble location-specific activity is effective and improves with experience. Decoding environment from cell-pair coactivity relationships is also effective and improves with experience, even after removing place tuning. Discriminating environments from 1-s ensemble coactivity relies crucially on the cells with the most anti-coactive cell-pair relationships because activity is internally organized on a low-dimensional manifold of non-linear coactivity relationships that intermittently reregisters to environments according to the anti-cofiring subpopulation activity.http://www.sciencedirect.com/science/article/pii/S2211124723011543CP: Neuroscience |
| spellingShingle | Eliott Robert Joseph Levy Simón Carrillo-Segura Eun Hye Park William Thomas Redman José Rafael Hurtado SueYeon Chung André Antonio Fenton A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields Cell Reports CP: Neuroscience |
| title | A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| title_full | A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| title_fullStr | A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| title_full_unstemmed | A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| title_short | A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| title_sort | manifold neural population code for space in hippocampal coactivity dynamics independent of place fields |
| topic | CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723011543 |
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