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Expectation violations enhance neuronal encoding of sensory information in mouse primary visual cortex

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Listed:
  • Matthew F. Tang

    (The Australian National University
    Australian Research Council Centre of Excellence for Integrative Brain Function
    The University of Queensland)

  • Ehsan Kheradpezhouh

    (The Australian National University
    Australian Research Council Centre of Excellence for Integrative Brain Function)

  • Conrad C. Y. Lee

    (The Australian National University
    Australian Research Council Centre of Excellence for Integrative Brain Function
    The University of Melbourne)

  • J. Edwin Dickinson

    (The University of Western Australia)

  • Jason B. Mattingley

    (Australian Research Council Centre of Excellence for Integrative Brain Function
    The University of Queensland
    The University of Queensland
    Canadian Institute for Advanced Research (CIFAR))

  • Ehsan Arabzadeh

    (The Australian National University
    Australian Research Council Centre of Excellence for Integrative Brain Function)

Abstract

The response of cortical neurons to sensory stimuli is shaped both by past events (adaptation) and the expectation of future events (prediction). Here we employed a visual stimulus paradigm with different levels of predictability to characterise how expectation influences orientation selectivity in the primary visual cortex (V1) of male mice. We recorded neuronal activity using two-photon calcium imaging (GCaMP6f) while animals viewed sequences of grating stimuli which either varied randomly in their orientations or rotated predictably with occasional transitions to an unexpected orientation. For single neurons and the population, there was significant enhancement in the gain of orientation-selective responses to unexpected gratings. This gain-enhancement for unexpected stimuli was prominent in both awake and anaesthetised mice. We implemented a computational model to demonstrate how trial-to-trial variability in neuronal responses were best characterised when adaptation and expectation effects were combined.

Suggested Citation

  • Matthew F. Tang & Ehsan Kheradpezhouh & Conrad C. Y. Lee & J. Edwin Dickinson & Jason B. Mattingley & Ehsan Arabzadeh, 2023. "Expectation violations enhance neuronal encoding of sensory information in mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36608-8
    DOI: 10.1038/s41467-023-36608-8
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    References listed on IDEAS

    as
    1. Miguel Maravall & Rasmus S Petersen & Adrienne L Fairhall & Ehsan Arabzadeh & Mathew E Diamond, 2007. "Shifts in Coding Properties and Maintenance of Information Transmission during Adaptation in Barrel Cortex," PLOS Biology, Public Library of Science, vol. 5(2), pages 1-12, January.
    2. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    3. Cooper A Smout & Matthew F Tang & Marta I Garrido & Jason B Mattingley, 2019. "Attention promotes the neural encoding of prediction errors," PLOS Biology, Public Library of Science, vol. 17(2), pages 1-22, February.
    4. Matthew F. Tang & Lucy Ford & Ehsan Arabzadeh & James T. Enns & Troy A. W. Visser & Jason B. Mattingley, 2020. "Neural dynamics of the attentional blink revealed by encoding orientation selectivity during rapid visual presentation," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. David M. Schneider & Janani Sundararajan & Richard Mooney, 2018. "A cortical filter that learns to suppress the acoustic consequences of movement," Nature, Nature, vol. 561(7723), pages 391-395, September.
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    Cited by:

    1. 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.

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