Vestibular and Multi-Sensory Influences Upon Self-Motion Perception and the Consequences for Human Behavior

Abstract

In this manuscript, we comprehensively review both the human and animal literature regarding vestibular and multi-sensory contributions to self-motion perception. This covers the anatomical basis and how and where the signals are processed at all levels from the peripheral vestibular system to the brainstem and cerebellum and finally to the cortex. Further, we consider how and where these vestibular signals are integrated with other sensory cues to facilitate self-motion perception. We conclude by demonstrating the wide-ranging influences of the vestibular system and self-motion perception upon behavior, namely eye movement, postural control, and spatial awareness as well as new discoveries that such perception can impact upon numerical cognition, human affect, and bodily self-consciousness.

Keywords: behavior; cerebellum; cortex; self-motion perception; vestibular system.

Figure 1

From section Perception of angular motion. This figure, modified from Grabherr et al. (43). Graph showing velocity thresholds as a function of sinusoidal motion frequency, where velocity is the peak velocity achieved in each cycle of sinusoidal acceleration. Black squares represent mean data from Grabherr et al. (43), n = 7. Left and right pointing triangles from Benson et al. (42), n = 6 and n = 8, respectively. Solid black line represents the fitted model for the high-pass filter K_TS/(TS + 1).

Figure 2

From section Perception of linear motion. This figure, modified from Gianna et al. (60). (A) Motion profiles for acceleration steps and corresponding rate of change of acceleration and velocity. (B) Acceleration thresholds for normal subjects (Ns) (mean +/– standard deviation) and individual subjects with vestibular impairment in the different conditions: step accelerations, low linear ramp (SlowR), high linear ramp (FastR), and parabolic acceleration (Par).

Figure 3

From section Prolonging self-motion perception: the velocity storage mechanism. This figure, from Okada et al. (84). (A) Eye velocity and vestibular sensation averaged across subjects (normal, n = 31, and congenital nystagmus, n = 14) after suddenly stopping whole-body passive rotations in the dark. (B) Mean duration, time constant and area under the curve of turning sensation in subjects with congenital nystagmus and healthy controls.

Figure 4

From section So where is self-motion perception processed? Diagram summarizing the main vestibular projections and brain regions contributing to self-motion perception. Dashed arrows indicate integration with extra-vestibular inputs.

Figure 5

From section Cerebellar contributions to self-motion perception. This Figure, from Bronstein et al. (102). (A) Graphs of representative individuals for perceived angular velocity after suddenly stopping rotations in the dark. (B) Median duration, time constant and area under the curve for sensation and eye velocity in patients with midline cerebellar degeneration (n = 8) and healthy controls (n = 8).

Figure 6

From section, The effect of self-motion perception on numerical magnitude allocation. This Figure, modified from Arshad et al. (306). Graph showing percentage error in the number bisection task (normalized to 0% error by subtracting the baseline) for the four perceptual conditions: world motion right and left and self-motion (vection) right and left. Box-plots represent the median and interquartile range with whiskers denoting 10th and 90th percentile. ^**Marks significance at p < 0.01.