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Revealing nonlinear neural decoding by analyzing choices

Author

Listed:
  • Qianli Yang

    (Rice University
    Aliyun School of Big Data
    Chinese Academy of Sciences)

  • Edgar Walker

    (Baylor College of Medicine
    Center for Neuroscience and Artificial Intelligence)

  • R. James Cotton

    (Shirley Ryan Ability Lab
    Northwestern University)

  • Andreas S. Tolias

    (Rice University
    Baylor College of Medicine
    Center for Neuroscience and Artificial Intelligence)

  • Xaq Pitkow

    (Rice University
    Baylor College of Medicine
    Center for Neuroscience and Artificial Intelligence)

Abstract

Sensory data about most natural task-relevant variables are entangled with task-irrelevant nuisance variables. The neurons that encode these relevant signals typically constitute a nonlinear population code. Here we present a theoretical framework for quantifying how the brain uses or decodes its nonlinear information. Our theory obeys fundamental mathematical limitations on information content inherited from the sensory periphery, describing redundant codes when there are many more cortical neurons than primary sensory neurons. The theory predicts that if the brain uses its nonlinear population codes optimally, then more informative patterns should be more correlated with choices. More specifically, the theory predicts a simple, easily computed quantitative relationship between fluctuating neural activity and behavioral choices that reveals the decoding efficiency. This relationship holds for optimal feedforward networks of modest complexity, when experiments are performed under natural nuisance variation. We analyze recordings from primary visual cortex of monkeys discriminating the distribution from which oriented stimuli were drawn, and find these data are consistent with the hypothesis of near-optimal nonlinear decoding.

Suggested Citation

  • Qianli Yang & Edgar Walker & R. James Cotton & Andreas S. Tolias & Xaq Pitkow, 2021. "Revealing nonlinear neural decoding by analyzing choices," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26793-9
    DOI: 10.1038/s41467-021-26793-9
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    References listed on IDEAS

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    1. 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.
    2. Yan Karklin & Michael S. Lewicki, 2009. "Emergence of complex cell properties by learning to generalize in natural scenes," Nature, Nature, vol. 457(7225), pages 83-86, January.
    3. Johannes Burge & Priyank Jaini, 2017. "Accuracy Maximization Analysis for Sensory-Perceptual Tasks: Computational Improvements, Filter Robustness, and Coding Advantages for Scaled Additive Noise," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-32, February.
    4. Kaushik J Lakshminarasimhan & Alexandre Pouget & Gregory C DeAngelis & Dora E Angelaki & Xaq Pitkow, 2018. "Inferring decoding strategies for multiple correlated neural populations," PLOS Computational Biology, Public Library of Science, vol. 14(9), pages 1-40, September.
    5. George H. Denfield & Alexander S. Ecker & Tori J. Shinn & Matthias Bethge & Andreas S. Tolias, 2018. "Attentional fluctuations induce shared variability in macaque primary visual cortex," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    6. Diego A. Gutnisky & Valentin Dragoi, 2008. "Adaptive coding of visual information in neural populations," Nature, Nature, vol. 452(7184), pages 220-224, March.
    7. Nicolas Pinto & David D Cox & James J DiCarlo, 2008. "Why is Real-World Visual Object Recognition Hard?," PLOS Computational Biology, Public Library of Science, vol. 4(1), pages 1-6, January.
    8. 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.
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    1. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.

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