Cited by 410Memory and Neural MechanismsSpatial Cognition and NavigationNeurogenesis and neuroplasticity mechanisms

Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments

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Frank, Loren M., Stanley, Garrett B., Brown, Emery N.·2004·The Journal of Neuroscience

Abstract

The hippocampus is essential for learning complex spatial relationships, but little is known about how hippocampal neural activity changes as animals learn about a novel environment. We studied the formation of new place representations in rats by examining the changes in place-specific firing of neurons in the CA1 region of the hippocampus and the relationship between these changes and behavioral change across multiple days of exposure to novel places. We found that many neurons showed very rapid changes on the first day of exposure to the novel place, including many cases in which a previously silent neuron developed a place field over the course of a single pass through the environment. Across the population, the largest changes in neural activity occurred on day 2 of exposure to a novel place, but only if the animal had little experience (<4 min) in that location on day 1. Longer exposures on day 1 were associated with smaller changes on day 2, suggesting that hippocampal neurons required 5-6 min of experience to form a stable spatial representation. Even after the representation stabilized, the animals' behavior remained different in the novel places, suggesting that other brain regions continued to distinguish novel from familiar locations. These results show that the hippocampus can form new spatial representations quickly but that stable hippocampal representations are not sufficient for a place to be treated as familiar.

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  • Firing associations between dCA1 pyramidal cells reorganized to represent each environment.

    “Additionally, we confirmed that firing associations between dCA1 pyramidal cells reorganized to represent each environment2,4,5,17(Supplementary Fig. 2a).”
  • New representations formed during exploration of novel environments or learning of new goal locations are initially labile and require stabilization to persist as memories.

    “However new representations, such as those formed during exploration of novel environments or learning of new goal locations, are initially labile and thus require stabilization to persist as memories4-6.”

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Authors
Frank, L. M., Stanley, G. B., & Brown, E. N.
Affiliations
  • Massachusetts General Hospital (US)
  • Harvard University (US)
Corresponding author
Brown, Emery N.
Venue
The Journal of Neuroscience
Published
2004-09-01
Volume
24
Issue
35
Pages
7681-7689
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2132611303
Cited by
410
References
50
Citations by year
2026: 4 · 2025: 28 · 2024: 26 · 2023: 23 · 2022: 20 · 2021: 25 · 2020: 17 · 2019: 33 · 2018: 16 · 2017: 12 · 2016: 21 · 2015: 13 · 2014: 18 · 2013: 23 · 2012: 18
FWCI
6.89
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (MH59733)
  • National Institute of Mental Health (MH65108, K02MH061637, MH59733, R01MH059733, F32MH065108, MH61673)
  • National Institute on Drug Abuse (DA015644, R01DA015644)
  • National Cancer Institute (R01CA094143)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
hippocampal plasticity, place cells, place fields, CA1, spatial learning, novel environment, representation of place, spatial memory, rats
MeSH terms
Animals, Environment, Exploratory Behavior, Habituation, Psychophysiologic, Hippocampus, Male, Memory, Neuronal Plasticity, Neurons, Reward, Spatial Behavior, Time Factors, Maze Learning, Rats, Long-Evans, Rats

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