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A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation

Author

Listed:
  • Hiroshi T. Ito

    (Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology)

  • Sheng-Jia Zhang

    (Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology)

  • Menno P. Witter

    (Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology)

  • Edvard I. Moser

    (Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology)

  • May-Britt Moser

    (Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology)

Abstract

Spatial navigation requires information about the relationship between current and future positions. The activity of hippocampal neurons appears to reflect such a relationship, representing not only instantaneous position but also the path towards a goal location. However, how the hippocampus obtains information about goal direction is poorly understood. Here we report a prefrontal–thalamic neural circuit that is required for hippocampal representation of routes or trajectories through the environment. Trajectory-dependent firing was observed in medial prefrontal cortex, the nucleus reuniens of the thalamus, and the CA1 region of the hippocampus in rats. Lesioning or optogenetic silencing of the nucleus reuniens substantially reduced trajectory-dependent CA1 firing. Trajectory-dependent activity was almost absent in CA3, which does not receive nucleus reuniens input. The data suggest that projections from medial prefrontal cortex, via the nucleus reuniens, are crucial for representation of the future path during goal-directed behaviour and point to the thalamus as a key node in networks for long-range communication between cortical regions involved in navigation.

Suggested Citation

  • Hiroshi T. Ito & Sheng-Jia Zhang & Menno P. Witter & Edvard I. Moser & May-Britt Moser, 2015. "A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation," Nature, Nature, vol. 522(7554), pages 50-55, June.
    • Handle: RePEc:nat:nature:v:522:y:2015:i:7554:d:10.1038_nature14396
    DOI: 10.1038/nature14396
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    Cited by:

    1. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. María P. Contreras & Marta Mendez & Xia Shan & Julia Fechner & Anuck Sawangjit & Jan Born & Marion Inostroza, 2024. "Context memory formed in medial prefrontal cortex during infancy enhances learning in adulthood," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Zihao Chen & Yechao Han & Zheng Ma & Xinnian Wang & Surui Xu & Yong Tang & Alexei L. Vyssotski & Bailu Si & Yang Zhan, 2024. "A prefrontal-thalamic circuit encodes social information for social recognition," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Jordan Crivelli-Decker & Alex Clarke & Seongmin A. Park & Derek J. Huffman & Erie D. Boorman & Charan Ranganath, 2023. "Goal-oriented representations in the human hippocampus during planning and navigation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Eleonora Russo & Nadine Becker & Aleks P. F. Domanski & Timothy Howe & Kipp Freud & Daniel Durstewitz & Matthew W. Jones, 2024. "Integration of rate and phase codes by hippocampal cell-assemblies supports flexible encoding of spatiotemporal context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Maanasa Jayachandran & Tatiana D. Viena & Andy Garcia & Abdiel Vasallo Veliz & Sofia Leyva & Valentina Roldan & Robert P. Vertes & Timothy A. Allen, 2023. "Nucleus reuniens transiently synchronizes memory networks at beta frequencies," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. G. Torromino & V. Loffredo & D. Cavezza & G. Sonsini & F. Esposito & A. H. Crevenna & M. Gioffrè & M. De Risi & A. Treves & M. Griguoli & E. De Leonibus, 2022. "Thalamo-hippocampal pathway regulates incidental memory capacity in mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Li Zheng & Zhiyao Gao & Andrew S. McAvan & Eve A. Isham & Arne D. Ekstrom, 2021. "Partially overlapping spatial environments trigger reinstatement in hippocampus and schema representations in prefrontal cortex," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    9. Toon Van de Maele & Bart Dhoedt & Tim Verbelen & Giovanni Pezzulo, 2024. "A hierarchical active inference model of spatial alternation tasks and the hippocampal-prefrontal circuit," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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