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Conjunctive encoding of exploratory intentions and spatial information in the hippocampus

Author

Listed:
  • Yi-Fan Zeng

    (ShanghaiTech University
    ShanghaiTech University)

  • Ke-Xin Yang

    (ShanghaiTech University)

  • Yilong Cui

    (ShanghaiTech University
    ShanghaiTech University)

  • Xiao-Na Zhu

    (ShanghaiTech University)

  • Rui Li

    (ShanghaiTech University
    ShanghaiTech University)

  • Hanqing Zhang

    (ShanghaiTech University)

  • Dong Chuan Wu

    (China Medical University
    China Medical University Hospital)

  • Raymond C. Stevens

    (ShanghaiTech University
    ShanghaiTech University)

  • Ji Hu

    (ShanghaiTech University
    ShanghaiTech University)

  • Ning Zhou

    (ShanghaiTech University)

Abstract

The hippocampus creates a cognitive map of the external environment by encoding spatial and self-motion-related information. However, it is unclear whether hippocampal neurons could also incorporate internal cognitive states reflecting an animal’s exploratory intention, which is not driven by rewards or unexpected sensory stimuli. In this study, a subgroup of CA1 neurons was found to encode both spatial information and animals’ investigatory intentions in male mice. These neurons became active before the initiation of exploration behaviors at specific locations and were nearly silent when the same fields were traversed without exploration. Interestingly, this neuronal activity could not be explained by object features, rewards, or mismatches in environmental cues. Inhibition of the lateral entorhinal cortex decreased the activity of these cells during exploration. Our findings demonstrate that hippocampal neurons may bridge external and internal signals, indicating a potential connection between spatial representation and intentional states in the construction of internal navigation systems.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47570-4
    DOI: 10.1038/s41467-024-47570-4
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    1. Denise J. Cai & Daniel Aharoni & Tristan Shuman & Justin Shobe & Jeremy Biane & Weilin Song & Brandon Wei & Michael Veshkini & Mimi La-Vu & Jerry Lou & Sergio E. Flores & Isaac Kim & Yoshitake Sano & , 2016. "A shared neural ensemble links distinct contextual memories encoded close in time," Nature, Nature, vol. 534(7605), pages 115-118, June.
    2. 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.
    3. Emma R. Wood & Paul A. Dudchenko & Howard Eichenbaum, 1999. "The global record of memory in hippocampal neuronal activity," Nature, Nature, vol. 397(6720), pages 613-616, February.
    4. Colin Lever & Tom Wills & Francesca Cacucci & Neil Burgess & John O'Keefe, 2002. "Long-term plasticity in hippocampal place-cell representation of environmental geometry," Nature, Nature, vol. 416(6876), pages 90-94, March.
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