How vestibular neurons solve the tilt/translation ambiguity. Comparison of brainstem, cerebellum, and thalamus

Abstract

The peripheral vestibular system is faced by a sensory ambiguity, where primary otolith afferents respond identically to translational (inertial) accelerations and changes in head orientation relative to gravity. Under certain conditions, this sensory ambiguity can be resolved using extra-otolith cues, including semicircular canal signals. Here we review and summarize how neurons in the vestibular nuclei, rostral fastigial nuclei, cerebellar nodulus/uvula, and thalamus respond during combinations of tilt and translation. We focus primarily on cerebellar cortex responses, as nodulus/uvula Purkinje cells reliably encode translation rather than net gravito-inertial acceleration. In contrast, neurons in the vestibular and rostral fastigial nuclei, as well as the ventral lateral and ventral posterior nuclei of the thalamus represent a continuum, with some encoding translation and some net gravito-inertial acceleration. This review also outlines how Purkinje cells use semicircular canal signals to solve the ambiguity problem and how this solution fails at low frequencies. We conclude by attempting to bridge the gap between the proposed roles of nodulus/uvula in tilt/translation discrimination and velocity storage.

Figure 1

Instantaneous firing rate of a typical Purkinje cell during (A) Translation, (B) Tilt, (C) Tilt − Translation, and (D) Tilt + Translation (0.5 Hz). The translation/tilt stimuli were matched in amplitude to elicit an identical net acceleration in the horizontal plane. Straight black and curved gray arrows denote translation and tilt axes of stimulation, respectively.

Figure 2

Scatter plots of partial correlation coefficients for fits of each cell responses with “translation-coding” and “afferent-like” models. (A) Data from NU Purkinje cells in labyrinthine-intact animals (filled circles) are compared with those in canal-plugged animals (open circles; both are replotted with permission from Yakusheva et al.29) and primary otolith afferents (AFF, open triangles; replotted with permission from Angelaki et al.1). (B) Data from vestibular nuclei neurons (replotted with permission from Angelaki et al.1). (C) Data from rostral fastigial nuclei neurons (replotted with permission from Angelaki et al.1). (D) Data from the ventral lateral and ventral posterior lateral nuclei of the thalamus (replotted with permission from Meng et al., © Journal of Neuroscience). The superimposed dashed lines divide the plots into three regions: an upper/left area corresponding to cell responses that were significantly better fit (P < 0.01) by the translation-coding model; a lower/right area that includes neurons that were significantly better fit by the afferent-like model; and an in-between area that would include cells that were not significantly better fit by either model. Data shown for the cell’s best-responding translation direction.

Figure 3

Spatio-temporal matching of canal-driven and otolith-driven signal contributions to NU Purkinje cell firing. (A), (B) Response amplitude and phase during the 0.5 Hz Tilt −Translation stimulus (canal-driven response) is plotted as a function of the respective amplitude and phase during Translation (otolith-driven response). (C) Distribution of the difference in preferred directions between the 0.5 Hz Tilt − “Translation and Translation responses. Data in A–C were replotted with permission from Yakusheva et al. (D), (E) Dependence of the relationship between otolith and canal-driven responses on frequency. (D) plots the ratio of peak response modulation during Tilt − Translation (canal-driven response) relative to that during Translation (otolith-driven response) as a function of frequency. (E) plots the phase difference between the response modulation during Tilt − Translation and Translation as a function of frequency. Thin lines and symbols illustrate data from single neurons, whereas thick lines indicate population averages. Data in D–E were replotted with permission from Yakusheva et al., © Journal of Neuroscience.

Figure 4

Schematic illustrating a hypothesis regarding the relationship between velocity storage and tilt/translation discrimination. Semicircular canal afferents carry head-referenced angular velocity (ω), but the NU encodes only the earth-horizontal component (ω_EH). Thus, because of Purkinje cell inhibition, NU-target neurons in the VN should carry the earth-vertical component (ω_EV = ω − ω_EH). Importantly, because the NU canal-driven responses are temporally integrated, VN responses are predicted to encode earth-vertical canal signals with a longer time constant than canal afferents. Replotted with permission from Yakusheva et al. © Journal of Neuroscience.