Abstract
We have previously reported that central neurons mediating vestibulo-spinal reflexes and self-motion perception optimally encode natural self-motion (Mitchell et al., 2018). Importantly however, the vestibular nuclei also comprise other neuronal classes that mediate essential functions such as the vestibulo-ocular reflex (VOR) and its adaptation. Here we show that heterogeneities in resting discharge variability mediate a trade-off between faithful encoding and optimal coding via temporal whitening. Specifically, neurons displaying lower variability did not whiten naturalistic self-motion but instead faithfully represented the stimulus' detailed time course, while neurons displaying higher variability displayed temporal whitening. Using a well-established model of VOR pathways, we demonstrate that faithful stimulus encoding is necessary to generate the compensatory eye movements found experimentally during naturalistic self-motion. Our findings suggest a novel functional role for variability toward establishing different coding strategies: (1) faithful stimulus encoding for generating the VOR; (2) optimized coding via temporal whitening for other vestibular functions.
Highlights
Our previous study was the first to investigate how neurons within the first central stage of vestibular processing in macaque monkeys respond to natural self-motion (Mitchell et al, 2018)
Our results revealed that VO neurons optimally encoded naturalistic self-motion stimuli through temporal whitening because both neuronal variability and tuning were matched to effectively complement natural stimulus statistics (Carriot et al, 2014; Carriot et al, 2017; Mitchell et al, 2018)
We investigated the effects of variability on the responses of three different central vestibular neuronal classes: neurons that mediate vestibulo-spinal pathways and project to the vestibular thalamus (i. e., VO), neurons that make the primary contribution to the vestibulo-ocular reflex (VOR) (i.e., PVP), and neurons that mediate VOR adaptation (i.e., EH)
Summary
Our previous study was the first to investigate how neurons within the first central stage of vestibular processing in macaque monkeys respond to natural self-motion (Mitchell et al, 2018). We focused on a class of neurons within the vestibular nuclei, vestibular-only (VO) neurons, that mediate vestibulo-spinal reflexes as well as self-motion perception (Abzug et al, 1974; Shinoda et al, 1988; Gdowski and McCrea, 1999; Meng et al, 2007; Marlinski and McCrea, 2009). While VO neurons mediate vestibulo-spinal reflexes as well as self-motion perception as mentioned above, two other distinct neuronal classes instead mediate the vestibulo-ocular reflex (VOR) and its adaptation.
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