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Sensory adaptation mediates efficient and unambiguous encoding of natural stimuli by vestibular thalamocortical pathways

Author

Listed:
  • Jerome Carriot

    (McGill University)

  • Graham McAllister

    (McGill University)

  • Hamed Hooshangnejad

    (Johns Hopkins University)

  • Isabelle Mackrous

    (McGill University)

  • Kathleen E. Cullen

    (Johns Hopkins University
    Johns Hopkins University School of Medicine
    Johns Hopkins University School of Medicine
    Johns Hopkins University)

  • Maurice J. Chacron

    (McGill University)

Abstract

Sensory systems must continuously adapt to optimally encode stimuli encountered within the natural environment. The prevailing view is that such optimal coding comes at the cost of increased ambiguity, yet to date, prior studies have focused on artificial stimuli. Accordingly, here we investigated whether such a trade-off between optimality and ambiguity exists in the encoding of natural stimuli in the vestibular system. We recorded vestibular nuclei and their target vestibular thalamocortical neurons during naturalistic and artificial self-motion stimulation. Surprisingly, we found no trade-off between optimality and ambiguity. Using computational methods, we demonstrate that thalamocortical neural adaptation in the form of contrast gain control actually reduces coding ambiguity without compromising the optimality of coding under naturalistic but not artificial stimulation. Thus, taken together, our results challenge the common wisdom that adaptation leads to ambiguity and instead suggest an essential role in underlying unambiguous optimized encoding of natural stimuli.

Suggested Citation

  • Jerome Carriot & Graham McAllister & Hamed Hooshangnejad & Isabelle Mackrous & Kathleen E. Cullen & Maurice J. Chacron, 2022. "Sensory adaptation mediates efficient and unambiguous encoding of natural stimuli by vestibular thalamocortical pathways," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30348-x
    DOI: 10.1038/s41467-022-30348-x
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    References listed on IDEAS

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    1. Diego A. Gutnisky & Valentin Dragoi, 2008. "Adaptive coding of visual information in neural populations," Nature, Nature, vol. 452(7184), pages 220-224, March.
    2. 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.
    3. Michael Lohse & Victoria M. Bajo & Andrew J. King & Ben D. B. Willmore, 2020. "Neural circuits underlying auditory contrast gain control and their perceptual implications," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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