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Hippocampal network reorganization underlies the formation of a temporal association memory

Mohsin S. Ahmed, View ORCID ProfileJames B. Priestley, Angel Castro, Fabio Stefanini, Elizabeth M. Balough, Erin Lavoie, Luca Mazzucato, Stefano Fusi, Attila Losonczy
doi: https://doi.org/10.1101/613638
Mohsin S. Ahmed
1Department of Psychiatry, Columbia University, New York, NY 10027 USA
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
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James B. Priestley
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
3Doctoral Program in Neurobiology and Behavior, Columbia University, New York, NY 10027 USA
4Center for Theoretical Neuroscience, Columbia University, New York, NY 10027 USA
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  • ORCID record for James B. Priestley
Angel Castro
1Department of Psychiatry, Columbia University, New York, NY 10027 USA
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
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Fabio Stefanini
3Doctoral Program in Neurobiology and Behavior, Columbia University, New York, NY 10027 USA
4Center for Theoretical Neuroscience, Columbia University, New York, NY 10027 USA
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Elizabeth M. Balough
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
3Doctoral Program in Neurobiology and Behavior, Columbia University, New York, NY 10027 USA
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Erin Lavoie
1Department of Psychiatry, Columbia University, New York, NY 10027 USA
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
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Luca Mazzucato
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
4Center for Theoretical Neuroscience, Columbia University, New York, NY 10027 USA
5Mortimer B. Zuckerman Mind Brain Behavior Institute Columbia University, New York, NY 10027 USA
6Departments of Mathematics and Biology University of Oregon, Eugene, OR 97403 USA
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Stefano Fusi
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
4Center for Theoretical Neuroscience, Columbia University, New York, NY 10027 USA
5Mortimer B. Zuckerman Mind Brain Behavior Institute Columbia University, New York, NY 10027 USA
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Attila Losonczy
2Department of Neuroscience, Columbia University, New York, NY 10027 USA
5Mortimer B. Zuckerman Mind Brain Behavior Institute Columbia University, New York, NY 10027 USA
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  • For correspondence: al2856@columbia.edu
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Abstract

Episodic memory requires linking events in time, a function dependent on the hippocampus. In “trace” fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use 2-photon calcium imaging to track neural population dynamics over the complete time-course of learning and show that, in contrast to previous theories, the hippocampus does not generate persistent activity to bridge the time delay. Instead, learning is concomitant with broad changes in the active neural population in CA1. While neural responses were highly stochastic in time, cue identity could be reliably read out from population activity rates over longer timescales after learning. These results question the ubiquity of neural sequences during temporal association learning, and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

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Posted April 18, 2019.
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Hippocampal network reorganization underlies the formation of a temporal association memory
Mohsin S. Ahmed, James B. Priestley, Angel Castro, Fabio Stefanini, Elizabeth M. Balough, Erin Lavoie, Luca Mazzucato, Stefano Fusi, Attila Losonczy
bioRxiv 613638; doi: https://doi.org/10.1101/613638
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Hippocampal network reorganization underlies the formation of a temporal association memory
Mohsin S. Ahmed, James B. Priestley, Angel Castro, Fabio Stefanini, Elizabeth M. Balough, Erin Lavoie, Luca Mazzucato, Stefano Fusi, Attila Losonczy
bioRxiv 613638; doi: https://doi.org/10.1101/613638

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