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Neural populations within macaque early vestibular pathways are adapted to encode natural self-motion

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  • Mohammad Mohammadi
  • Jerome Carriot
  • Isabelle Mackrous
  • Kathleen E Cullen
  • Maurice J Chacron

Abstract

How the activities of large neural populations are integrated in the brain to ensure accurate perception and behavior remains a central problem in systems neuroscience. Here, we investigated population coding of naturalistic self-motion by neurons within early vestibular pathways in rhesus macaques (Macacca mulatta). While vestibular neurons displayed similar dynamic tuning to self-motion, inspection of their spike trains revealed significant heterogeneity. Further analysis revealed that, during natural but not artificial stimulation, heterogeneity resulted primarily from variability across neurons as opposed to trial-to-trial variability. Interestingly, vestibular neurons displayed different correlation structures during naturalistic and artificial self-motion. Specifically, while correlations due to the stimulus (i.e., signal correlations) did not differ, correlations between the trial-to-trial variabilities of neural responses (i.e., noise correlations) were instead significantly positive during naturalistic but not artificial stimulation. Using computational modeling, we show that positive noise correlations during naturalistic stimulation benefits information transmission by heterogeneous vestibular neural populations. Taken together, our results provide evidence that neurons within early vestibular pathways are adapted to the statistics of natural self-motion stimuli at the population level. We suggest that similar adaptations will be found in other systems and species.Information about self-motion is detected by the vestibular end organs but how neural populations represent natural self-motion stimuli is unclear. This study shows that, in macaques, neurons in early vestibular pathways are adapted to the statistics of natural self-motion stimuli at the population level.

Suggested Citation

  • Mohammad Mohammadi & Jerome Carriot & Isabelle Mackrous & Kathleen E Cullen & Maurice J Chacron, 2024. "Neural populations within macaque early vestibular pathways are adapted to encode natural self-motion," PLOS Biology, Public Library of Science, vol. 22(4), pages 1-34, April.
    • Handle: RePEc:plo:pbio00:3002623
    DOI: 10.1371/journal.pbio.3002623
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    References listed on IDEAS

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    2. Jaime de la Rocha & Brent Doiron & Eric Shea-Brown & Krešimir Josić & Alex Reyes, 2007. "Correlation between neural spike trains increases with firing rate," Nature, Nature, vol. 448(7155), pages 802-806, August.
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