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Preexisting hippocampal network dynamics constrain optogenetically induced place fields

View ORCID ProfileSam McKenzie, Roman Huszár, Daniel F. English, Kanghwan Kim, Euisik Yoon, György Buzsáki
doi: https://doi.org/10.1101/803577
Sam McKenzie
1The Neuroscience Institute, Department of Neurology, NYU Langone Medical Center and Center for Neural Science, New York, NY
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  • ORCID record for Sam McKenzie
Roman Huszár
1The Neuroscience Institute, Department of Neurology, NYU Langone Medical Center and Center for Neural Science, New York, NY
2Center for Neural Science, New York University, 4 Washington Pl, New York, NY 10003, USA
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Daniel F. English
1The Neuroscience Institute, Department of Neurology, NYU Langone Medical Center and Center for Neural Science, New York, NY
3Virginia Polytechnic Institute and State University, Blacksburg, VA
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Kanghwan Kim
4Department of Electrical Engineering and Computer Science, University of Michigan, Ann Arbor, MI
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Euisik Yoon
4Department of Electrical Engineering and Computer Science, University of Michigan, Ann Arbor, MI
5Center for Nanomedicine, Institute for Basic Science (IBS) and Graduate Program of Nano Biomedical Engineering (Nano BME), Yonsei University, Seoul 03722, Republic of Korea
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György Buzsáki
1The Neuroscience Institute, Department of Neurology, NYU Langone Medical Center and Center for Neural Science, New York, NY
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  • For correspondence: gyorgy.buzsaki@nyumc.org
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Summary

Neuronal circuits face a fundamental tension between maintaining existing structure and changing to accommodate new information. Memory models often emphasize the need to encode novel patterns of neural activity imposed by “bottom-up” sensory drive. In such models, learning is achieved through synaptic alterations, a process which potentially interferes with previously stored knowledge 1-3. Alternatively, neuronal circuits generate and maintain a preconfigured stable dynamic, sometimes referred to as an attractor, manifold, or schema 4-7, with a large reservoir of patterns available for matching with novel experiences 8-13. Here, we show that incorporation of arbitrary signals is constrained by pre-existing circuit dynamics. We optogenetically stimulated small groups of hippocampal neurons as mice traversed a chosen segment of a linear track, mimicking the emergence of place fields 1,14,15, while simultaneously recording the activity of stimulated and non-stimulated neighboring cells. Stimulation of principal neurons in CA1, but less so CA3 or the dentate gyrus, induced persistent place field remapping. Novel place fields emerged in both stimulated and non-stimulated neurons, which could be predicted from sporadic firing in the new place field location and the temporal relationship to peer neurons prior to the optogenetic perturbation. Circuit modification was reflected by altered spike transmission between connected pyramidal cell – inhibitory interneuron pairs, which persisted during post-experience sleep. We hypothesize that optogenetic perturbation unmasked sub-threshold, pre-existing place fields16,17. Plasticity in recurrent/lateral inhibition may drive learning through rapid exploration of existing states.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 13, 2019.
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Preexisting hippocampal network dynamics constrain optogenetically induced place fields
Sam McKenzie, Roman Huszár, Daniel F. English, Kanghwan Kim, Euisik Yoon, György Buzsáki
bioRxiv 803577; doi: https://doi.org/10.1101/803577
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Preexisting hippocampal network dynamics constrain optogenetically induced place fields
Sam McKenzie, Roman Huszár, Daniel F. English, Kanghwan Kim, Euisik Yoon, György Buzsáki
bioRxiv 803577; doi: https://doi.org/10.1101/803577

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