Xiong-Jie Yu

Long-term deficits in motion detection thresholds and spike count variability after unilateral vestibular lesion

The vestibular system operates in a push-pull fashion using signals from both labyrinths and an intricate bilateral organization. Unilateral vestibular lesions cause well-characterized motor deficits that are partially compensated over time and whose neural correlates have been traced in the mean response modulation of vestibular nuclei cells. Here we compare both response gains and neural detection thresholds of vestibular nuclei and semicircular canal afferent neurons in intact vs. unilateral-lesioned macaques using three-dimensional rotation and translation stimuli. We found increased stimulus-driven spike count variability and detection thresholds in semicircular canal afferents, although mean responses were unchanged, after contralateral labyrinth lesion. Analysis of trial-by-trial spike count correlations of a limited number of simultaneously recorded pairs of canal afferents suggests increased noise correlations after lesion. In addition, we also found persistent, chronic deficits in rotation detection thresholds of vestibular nuclei neurons, which were larger in the ipsilesional than the contralesional brain stem. These deficits, which persisted several months after lesion, were due to lower rotational response gains, whereas spike count variability was similar in intact and lesioned animals. In contrast to persistent deficits in rotation threshold, translation detection thresholds were not different from those in intact animals. These findings suggest that, after compensation, a single labyrinth is sufficient to recover motion sensitivity and normal thresholds for the otolith, but not the semicircular canal, system.

Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents with neurons in the vestibular and cerebellar nuclei, as well as five cortical areas, to identical three-dimensional translational motion. We demonstrate a remarkable spatio-temporal transformation: otolith afferents carry spatially aligned cosine-tuned translational acceleration and jerk signals. In contrast, brainstem and cerebellar neurons exhibit non-linear, mixed selectivity for translational velocity, acceleration, jerk and position. Furthermore, these components often show dissimilar spatial tuning. Moderate further transformation of translation signals occurs in the cortex, such that similar spatio-temporal properties are found in multiple cortical areas. These results suggest that the first synapse represents a key processing element in vestibular pathways, robustly shaping how self-motion is represented in central vestibular circuits and cortical areas. DOI: http://dx.doi.org/10.7554/eLife.20787.001