Latent learning drives sleep-dependent plasticity in distinct CA1 subpopulations

Latent learning is a process that enables the brain to transform experiences into "cognitive maps," a form of implicit memory, without requiring reinforced training. To investigate its neural mechanisms, we record from hippocampal neurons in mice during latent learning of spatial maps and observe that the high-dimensional neural state space gradually transforms into a low-dimensional manifold that closely resembles the physical environment. This transformation process is associated with the neural reactivation of navigational experiences during sleep. Additionally, we identify a subset of hippocampal neurons that, rather than forming place fields in a novel environment, maintain weak spatial tuning but gradually develop correlated activity with other neurons. The elevated correlation introduces redundancy into the ensemble code, transforming the neural state space into a low-dimensional manifold that effectively links discrete place fields of place cells into a map-like structure. These results suggest a potential mechanism for latent learning of spatial maps in the hippocampus.

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Publication Details

Journal
Cell Reports
Published
2024-11-28
DOI
https://doi.org/10.1016/j.celrep.2024.115028
Citations
6
Primary Topic
Sleep and Wakefulness Research
Type
article
Field-Weighted Citation Impact
2.06

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article

Latent learning drives sleep-dependent plasticity in distinct CA1 subpopulations

Jonathan P. Newman, Jie Zhang, Wei Guo, Matthew A. Wilson
6 citations
Cell Reports
Sleep and Wakefulness Research
2.06
article

Latent learning drives sleep-dependent plasticity in distinct CA1 subpopulations

Jonathan P. Newman, Jie Zhang, Wei Guo, Matthew A. Wilson
article en
6 citations

Abstract

Latent learning is a process that enables the brain to transform experiences into "cognitive maps," a form of implicit memory, without requiring reinforced training. To investigate its neural mechanisms, we record from hippocampal neurons in mice during latent learning of spatial maps and observe that the high-dimensional neural state space gradually transforms into a low-dimensional manifold that closely resembles the physical environment. This transformation process is associated with the neural reactivation of navigational experiences during sleep. Additionally, we identify a subset of hippocampal neurons that, rather than forming place fields in a novel environment, maintain weak spatial tuning but gradually develop correlated activity with other neurons. The elevated correlation introduces redundancy into the ensemble code, transforming the neural state space into a low-dimensional manifold that effectively links discrete place fields of place cells into a map-like structure. These results suggest a potential mechanism for latent learning of spatial maps in the hippocampus.

Cell ReportsVol. 43(12)
Open Geospatial Consortium (US), Massachusetts Institute of Technology (US)
Foundation for the National Institutes of Health, Israel National Road Safety Authority, National Institutes of Health
Openalex Percentile: Top 13%
Sleep and Wakefulness Research
2.06
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Latent learning drives sleep-dependent plasticity in distinct CA1 subpopulations — Jonathan P. Newman, Jie Zhang, et al. · Cell Reports (2024) | TGRS Research Map | TGRS