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Projections from neocortex mediate top-down control of memory retrieval

Author

Listed:
  • Priyamvada Rajasethupathy

    (Stanford University
    CNC Program, Stanford University)

  • Sethuraman Sankaran

    (CNC Program, Stanford University)

  • James H. Marshel

    (Stanford University)

  • Christina K. Kim

    (Stanford University
    Neuroscience Program, Stanford University)

  • Emily Ferenczi

    (Stanford University
    Neuroscience Program, Stanford University)

  • Soo Yeun Lee

    (Stanford University
    Neuroscience Program, Stanford University)

  • Andre Berndt

    (Stanford University
    Neuroscience Program, Stanford University)

  • Charu Ramakrishnan

    (Stanford University)

  • Anna Jaffe

    (Stanford University)

  • Maisie Lo

    (Stanford University)

  • Conor Liston

    (Stanford University
    Stanford University)

  • Karl Deisseroth

    (Stanford University
    CNC Program, Stanford University
    Stanford University
    Howard Hughes Medical Institute, Stanford University)

Abstract

Top-down prefrontal cortex inputs to the hippocampus have been hypothesized to be important in memory consolidation, retrieval, and the pathophysiology of major psychiatric diseases; however, no such direct projections have been identified and functionally described. Here we report the discovery of a monosynaptic prefrontal cortex (predominantly anterior cingulate) to hippocampus (CA3 to CA1 region) projection in mice, and find that optogenetic manipulation of this projection (here termed AC–CA) is capable of eliciting contextual memory retrieval. To explore the network mechanisms of this process, we developed and applied tools to observe cellular-resolution neural activity in the hippocampus while stimulating AC–CA projections during memory retrieval in mice behaving in virtual-reality environments. Using this approach, we found that learning drives the emergence of a sparse class of neurons in CA2/CA3 that are highly correlated with the local network and that lead synchronous population activity events; these neurons are then preferentially recruited by the AC–CA projection during memory retrieval. These findings reveal a sparsely implemented memory retrieval mechanism in the hippocampus that operates via direct top-down prefrontal input, with implications for the patterning and storage of salient memory representations.

Suggested Citation

  • Priyamvada Rajasethupathy & Sethuraman Sankaran & James H. Marshel & Christina K. Kim & Emily Ferenczi & Soo Yeun Lee & Andre Berndt & Charu Ramakrishnan & Anna Jaffe & Maisie Lo & Conor Liston & Karl, 2015. "Projections from neocortex mediate top-down control of memory retrieval," Nature, Nature, vol. 526(7575), pages 653-659, October.
  • Handle: RePEc:nat:nature:v:526:y:2015:i:7575:d:10.1038_nature15389
    DOI: 10.1038/nature15389
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    Cited by:

    1. Jens Leth Hougaard & Juan D. Moreno-Ternero & Lars Peter Østerdal, 2022. "Optimal Management of Evolving Hierarchies," Management Science, INFORMS, vol. 68(8), pages 6024-6038, August.
    2. 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.
    3. Thomas Hainmueller & Aurore Cazala & Li-Wen Huang & Marlene Bartos, 2024. "Subfield-specific interneuron circuits govern the hippocampal response to novelty in male mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Robert N. Fetcho & Baila S. Hall & David J. Estrin & Alexander P. Walsh & Peter J. Schuette & Jesse Kaminsky & Ashna Singh & Jacob Roshgodal & Charlotte C. Bavley & Viraj Nadkarni & Susan Antigua & Th, 2023. "Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    6. Vinod Menon & Domenic Cerri & Byeongwook Lee & Rui Yuan & Sung-Ho Lee & Yen-Yu Ian Shih, 2023. "Optogenetic stimulation of anterior insular cortex neurons in male rats reveals causal mechanisms underlying suppression of the default mode network by the salience network," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Brent Kevin Young & Jayden Nicole Brennan & Ping Wang & Ning Tian, 2018. "Virtual reality method to analyze visual recognition in mice," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-14, May.
    8. Heather C. Ratigan & Seetha Krishnan & Shai Smith & Mark E. J. Sheffield, 2023. "A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Arita Silapetere & Songhwan Hwang & Yusaku Hontani & Rodrigo G. Fernandez Lahore & Jens Balke & Francisco Velazquez Escobar & Martijn Tros & Patrick E. Konold & Rainer Matis & Roberta Croce & Peter J., 2022. "QuasAr Odyssey: the origin of fluorescence and its voltage sensitivity in microbial rhodopsins," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    10. Rodrigo G. Fernandez Lahore & Niccolò P. Pampaloni & Enrico Schiewer & M.-Marcel Heim & Linda Tillert & Johannes Vierock & Johannes Oppermann & Jakob Walther & Dietmar Schmitz & David Owald & Andrew J, 2022. "Calcium-permeable channelrhodopsins for the photocontrol of calcium signalling," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    11. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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