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Feature-specific prediction errors and surprise across macaque fronto-striatal circuits

Author

Listed:
  • Mariann Oemisch

    (York University
    Yale University School of Medicine)

  • Stephanie Westendorff

    (York University
    University of Tübingen)

  • Marzyeh Azimi

    (York University)

  • Seyed Alireza Hassani

    (York University
    Vanderbilt University)

  • Salva Ardid

    (Boston University)

  • Paul Tiesinga

    (Radboud University Nijmegen)

  • Thilo Womelsdorf

    (York University
    Vanderbilt University)

Abstract

To adjust expectations efficiently, prediction errors need to be associated with the precise features that gave rise to the unexpected outcome, but this credit assignment may be problematic if stimuli differ on multiple dimensions and it is ambiguous which feature dimension caused the outcome. Here, we report a potential solution: neurons in four recorded areas of the anterior fronto-striatal networks encode prediction errors that are specific to feature values of different dimensions of attended multidimensional stimuli. The most ubiquitous prediction error occurred for the reward-relevant dimension. Feature-specific prediction error signals a) emerge on average shortly after non-specific prediction error signals, b) arise earliest in the anterior cingulate cortex and later in dorsolateral prefrontal cortex, caudate and ventral striatum, and c) contribute to feature-based stimulus selection after learning. Thus, a widely-distributed feature-specific eligibility trace may be used to update synaptic weights for improved feature-based attention.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-018-08184-9
    DOI: 10.1038/s41467-018-08184-9
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    Cited by:

    1. Francesco Ceccarelli & Lorenzo Ferrucci & Fabrizio Londei & Surabhi Ramawat & Emiliano Brunamonti & Aldo Genovesio, 2023. "Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Shiva Farashahi & Alireza Soltani, 2021. "Computational mechanisms of distributed value representations and mixed learning strategies," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    3. Tarana Nigam & Caspar M. Schwiedrzik, 2024. "Predictions enable top-down pattern separation in the macaque face-processing hierarchy," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. 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.

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