The Increased Sensitivity of Irregular Peripheral Canal and Otolith Vestibular Afferents Optimizes their Encoding of Natural Stimuli

Abstract

Efficient processing of incoming sensory input is essential for an organism's survival. A growing body of evidence suggests that sensory systems have developed coding strategies that are constrained by the statistics of the natural environment. Consequently, it is necessary to first characterize neural responses to natural stimuli to uncover the coding strategies used by a given sensory system. Here we report for the first time the statistics of vestibular rotational and translational stimuli experienced by rhesus monkeys during natural (e.g., walking, grooming) behaviors. We find that these stimuli can reach intensities as high as 1500 deg/s and 8 G. Recordings from afferents during naturalistic rotational and linear motion further revealed strongly nonlinear responses in the form of rectification and saturation, which could not be accurately predicted by traditional linear models of vestibular processing. Accordingly, we used linear-nonlinear cascade models and found that these could accurately predict responses to naturalistic stimuli. Finally, we tested whether the statistics of natural vestibular signals constrain the neural coding strategies used by peripheral afferents. We found that both irregular otolith and semicircular canal afferents, because of their higher sensitivities, were more optimized for processing natural vestibular stimuli as compared with their regular counterparts. Our results therefore provide the first evidence supporting the hypothesis that the neural coding strategies used by the vestibular system are matched to the statistics of natural stimuli.

The statistics of the vestibular input experienced during natural self‐motion differ between rodents and primates

“…The dataset was the same as that previously published (Schneider et al . ); however, we note that Schneider et al . () did not consider the spectral content of the recorded signals.…”

Self-motion evokes precise spike timing in the primate vestibular system

“…Indeed, this view is supported by numerous studies showing that both afferents and central neurons accurately encode the detailed time course of head rotations through linearly related changes in firing rate over a wide range of frequencies reviewed in refs 1, 5, 29. Moreover, prior investigations had established that both peripheral30 and central28 vestibular neurons can respond nonlinearly to single repetitions of naturalistic stimuli14. However, while this property is required for temporal coding, it is not sufficient.…”

“…We note that the stimuli used in the present study do not elicit simple (that is, rectification, saturation) static nonlinearities in either regular or irregular afferents530. To detect the presence of other nonlinearities in the response, we quantified correlations between the neuronal response R(t) and the stimulus S(t) using the stimulus-response (SR) coherence C SR (f) , as in ref.…”

“…To account for the known response dynamics of both regular and irregular semicircular canal afferents, the stimulus S ( t ) used in the model was obtained by filtering the original broadband noise current using the transfer functions of regular and irregular units as done previously30. The parameters σ noise and σ signal determine the response variability and the strength of the signal, respectively.…”

Cerebellar re-encoding of self-generated head movements

“…However, these movements only covered the lower range of frequencies and amplitudes observed during active self-motion (Carriot et al, 2015). Moreover, despite the remarkable linearity of early vestibular information processing (Bagnall et al, 2008), the high amplitude of active movements might recruit vestibular afferents in a non-linear way (Schneider et al, 2015). In addition, studies in mice and monkeys have revealed that active and passive head movements are processed in fundamentally different ways within the vestibular nuclei (Cullen & Roy, 2004), which are highly interconnected with the caudal cerebellar vermis.…”