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Geometry of abstract learned knowledge in the hippocampus

Author

Listed:
  • Edward H. Nieh

    (Princeton University)

  • Manuel Schottdorf

    (Princeton University)

  • Nicolas W. Freeman

    (Princeton University)

  • Ryan J. Low

    (Princeton University)

  • Sam Lewallen

    (Princeton University)

  • Sue Ann Koay

    (Princeton University)

  • Lucas Pinto

    (Princeton University
    Northwestern University)

  • Jeffrey L. Gauthier

    (Princeton University)

  • Carlos D. Brody

    (Princeton University
    Princeton University
    Princeton University)

  • David W. Tank

    (Princeton University
    Princeton University
    Princeton University)

Abstract

Hippocampal neurons encode physical variables1–7 such as space1 or auditory frequency6 in cognitive maps8. In addition, functional magnetic resonance imaging studies in humans have shown that the hippocampus can also encode more abstract, learned variables9–11. However, their integration into existing neural representations of physical variables12,13 is unknown. Here, using two-photon calcium imaging, we show that individual neurons in the dorsal hippocampus jointly encode accumulated evidence with spatial position in mice performing a decision-making task in virtual reality14–16. Nonlinear dimensionality reduction13 showed that population activity was well-described by approximately four to six latent variables, which suggests that neural activity is constrained to a low-dimensional manifold. Within this low-dimensional space, both physical and abstract variables were jointly mapped in an orderly manner, creating a geometric representation that we show is similar across mice. The existence of conjoined cognitive maps suggests that the hippocampus performs a general computation—the creation of task-specific low-dimensional manifolds that contain a geometric representation of learned knowledge.

Suggested Citation

  • Edward H. Nieh & Manuel Schottdorf & Nicolas W. Freeman & Ryan J. Low & Sam Lewallen & Sue Ann Koay & Lucas Pinto & Jeffrey L. Gauthier & Carlos D. Brody & David W. Tank, 2021. "Geometry of abstract learned knowledge in the hippocampus," Nature, Nature, vol. 595(7865), pages 80-84, July.
  • Handle: RePEc:nat:nature:v:595:y:2021:i:7865:d:10.1038_s41586-021-03652-7
    DOI: 10.1038/s41586-021-03652-7
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    Citations

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    Cited by:

    1. Joanna C. Chang & Matthew G. Perich & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2024. "De novo motor learning creates structure in neural activity that shapes adaptation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Valeria Fascianelli & Aldo Battista & Fabio Stefanini & Satoshi Tsujimoto & Aldo Genovesio & Stefano Fusi, 2024. "Neural representational geometries reflect behavioral differences in monkeys and recurrent neural networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Eleanor Spens & Neil Burgess, 2024. "A generative model of memory construction and consolidation," Nature Human Behaviour, Nature, vol. 8(3), pages 526-543, March.
    4. Eunji Kong & Kyu-Hee Lee & Jongrok Do & Pilhan Kim & Doyun Lee, 2023. "Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Yi-Fan Zeng & Ke-Xin Yang & Yilong Cui & Xiao-Na Zhu & Rui Li & Hanqing Zhang & Dong Chuan Wu & Raymond C. Stevens & Ji Hu & Ning Zhou, 2024. "Conjunctive encoding of exploratory intentions and spatial information in the hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Changyuan Yang & Sai Ma & Qinkai Han, 2023. "Unified discriminant manifold learning for rotating machinery fault diagnosis," Journal of Intelligent Manufacturing, Springer, vol. 34(8), pages 3483-3494, December.
    7. Ian Cone & Claudia Clopath, 2024. "Latent representations in hippocampal network model co-evolve with behavioral exploration of task structure," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Huixin Lin & Jingfeng Zhou, 2024. "Hippocampal and orbitofrontal neurons contribute to complementary aspects of associative structure," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. P. Dylan Rich & Stephan Yves Thiberge & Benjamin B. Scott & Caiying Guo & D. Gowanlock R. Tervo & Carlos D. Brody & Alla Y. Karpova & Nathaniel D. Daw & David W. Tank, 2024. "Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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