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Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences

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Priestley, James B., Bowler, John C., Rolotti, Sebi V., Fusi, Stefano, Losonczy, Attila·2022·Neuron
DOI 10.1016/j.neuron.2022.03.026PMC PMC9233041

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Abstract

Neurons in the hippocampus exhibit a striking selectivity for specific combinations of sensory features, forming representations that are thought to subserve episodic memory. Even during completely novel experiences, hippocampal "place cells" are rapidly configured such that the population sparsely encodes visited locations, stabilizing within minutes of the first exposure to a new environment. What mechanisms enable this fast encoding of experience? Using virtual reality and neural population recordings in mice, we dissected the effects of novelty and experience on the dynamics of place field formation. During place field formation, many CA1 neurons immediately modulated the amplitude of their activity and shifted the location of their field, rapid changes in tuning predicted by behavioral timescale synaptic plasticity (BTSP). Signatures of BTSP were particularly enriched during the exploration of a novel context and decayed with experience. Our data suggest that novelty modulates the effective learning rate in CA1, favoring rapid mechanisms of field formation to encode a new experience.

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  • Behavioral timescale synaptic plasticity (BTSP) is responsible for the rapid formation of hippocampal place fields.

    “behavioral timescale synaptic plasticity (BTSP) (103–106), which is responsible for the rapid formation of hippocampal place fields.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [105]

    The Discussion says the results are consistent with a sizable fraction of de novo place fields forming via BTSP, particularly during novel experiences. The claim states this as an established causal role in rapid place-field formation, whereas the paper describes indirect correlates and acknowledges that fields can form through other mechanisms. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • BTSP is NMDAR dependent and, unlike classical LTP, has a coincidence time window of seconds rather than milliseconds.

    “It is NMDAR dependent, but unlike classical LTP the coincidence time window is seconds, not milliseconds.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [105]

    The Introduction (page unavailable) says BTSP affects inputs active several seconds before a burst and calls it a departure from conventional plasticity schemes, supporting the seconds-scale distinction. The available passages do not state that BTSP is NMDAR dependent or explicitly quantify classical LTP’s window in milliseconds. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

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Cited by

Sorted by citations

Authors
Priestley, J. B., Bowler, J. C., Rolotti, S. V., Fusi, S., & Losonczy, A.
Affiliations
  • Columbia University (US)
  • Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
Corresponding author
  • Priestley, James B.
  • Losonczy, Attila
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2022-06
Volume
110
Issue
12
Pages
1978-1992.e6
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2022.03.026
PMC
PMC9233041
OpenAlex
W4224232972
Cited by
122
References
8
Citations by year
2026: 23 · 2025: 37 · 2024: 34 · 2023: 20 · 2022: 8
FWCI
12.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • DARPA (DBI-1707398)
  • Simons Foundation
  • National Institute of Mental Health (1R01MH124867, 1R01MH124047, F31MH121058, 1U01NS115530, 1R01NS121106, 1U19NS104590, F31NS110316, F31MH117892)
  • National Science Foundation
  • Gatsby Charitable Foundation
  • National Institute of Neurological Disorders and Stroke
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
hippocampal CA1, place cells, novelty, learning rate, virtual reality, spatial representation, episodic memory, mice
MeSH terms
Place Cells, Animals, Hippocampus, Learning, Neuronal Plasticity, Neurons, Mice, CA1 Region, Hippocampal

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