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Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex in mice during decision making

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  • Márton Albert Hajnal

    (HUN-REN Wigner Research Centre for Physics)

  • Duy Tran

    (University of California, Los Angeles
    Albert Einstein College of Medicine)

  • Zsombor Szabó

    (HUN-REN Wigner Research Centre for Physics)

  • Andrea Albert

    (HUN-REN Wigner Research Centre for Physics)

  • Karen Safaryan

    (University of California, Los Angeles)

  • Michael Einstein

    (University of California, Los Angeles)

  • Mauricio Vallejo Martelo

    (University of California, Los Angeles)

  • Pierre-Olivier Polack

    (Rutgers University)

  • Peyman Golshani

    (University of California, Los Angeles
    University of California, Los Angeles
    West Los Angeles VA Medical Center)

  • Gergő Orbán

    (HUN-REN Wigner Research Centre for Physics)

Abstract

Attention supports decision making by selecting the features that are relevant for decisions. Selective enhancement of the relevant features and inhibition of distractors has been proposed as potential neural mechanisms driving this selection process. Yet, how attention operates when relevance cannot be directly determined, and the attention signal needs to be internally constructed is less understood. Here we recorded from populations of neurons in the anterior cingulate cortex (ACC) of mice in an attention-shifting task where relevance of stimulus modalities changed across blocks of trials. In contrast with V1 recordings, decoding of the irrelevant modality gradually declined in ACC after an initial transient. Our analytical proof and a recurrent neural network model of the task revealed mutually inhibiting connections that produced context-gated suppression as observed in mice. Using this RNN model we predicted a correlation between contextual modulation of individual neurons and their stimulus drive, which we confirmed in ACC but not in V1.

Suggested Citation

  • Márton Albert Hajnal & Duy Tran & Zsombor Szabó & Andrea Albert & Karen Safaryan & Michael Einstein & Mauricio Vallejo Martelo & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2024. "Shifts in attention drive context-dependent subspace encoding in anterior cingulate cortex in mice during decision making," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49845-2
    DOI: 10.1038/s41467-024-49845-2
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    References listed on IDEAS

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    1. Nir Moneta & Mona M. Garvert & Hauke R. Heekeren & Nicolas W. Schuck, 2023. "Task state representations in vmPFC mediate relevant and irrelevant value signals and their behavioral influence," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    3. James B. Heald & Máté Lengyel & Daniel M. Wolpert, 2021. "Contextual inference underlies the learning of sensorimotor repertoires," Nature, Nature, vol. 600(7889), pages 489-493, December.
    4. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    5. Márton Albert Hajnal & Duy Tran & Michael Einstein & Mauricio Vallejo Martelo & Karen Safaryan & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2023. "Continuous multiplexed population representations of task context in the mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Mariann Oemisch & Stephanie Westendorff & Marzyeh Azimi & Seyed Alireza Hassani & Salva Ardid & Paul Tiesinga & Thilo Womelsdorf, 2019. "Feature-specific prediction errors and surprise across macaque fronto-striatal circuits," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Athena Akrami & Charles D. Kopec & Mathew E. Diamond & Carlos D. Brody, 2018. "Posterior parietal cortex represents sensory history and mediates its effects on behaviour," Nature, Nature, vol. 554(7692), pages 368-372, February.
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