Gravity or translation: Central processing of vestibular signals to detect motion or tilt

The processing and detection of tilts relative to gravity from actual motion (translational accelerations) is one of the most fundamental issues for understanding vestibular sensorimotor control in altered gravity environments. In order to better understand the nature of multisensory signals in detecting motion and tilt, we summarize here our recent studies regarding the central processing of vestibular signals during multi-axis rotational and translational stimuli. Approximately one fourth of the cells in the vestibular nuclei exclusively encoded rotational movements (Canal-Only neurons) and were unresponsive to translation. The Canal-Only central neurons encoded head rotation in canal afferent coordinates, exhibited no orthogonal canal convergence and were characterized by significantly higher sensitivities to rotation as compared to canal afferents. Another fourth of the neurons modulated their firing rates during translation (Otolith-Only cells). During rotations, these neurons typically only responded when the axis of rotation was earth-horizontal and the head was changing orientation relative to gravity. The remaining cells (approximately half of total population) were sensitive to both rotations and translations (Otolith+Canal neurons). Maximum sensitivity vectors to rotation were distributed throughout the 3D space, suggesting strong convergence from multiple semicircular canals. Only a small subpopulation (approximately one third) of these Otolith+Canal neurons seems to encode a true estimate of the translational component of the imposed passive head and body movement. These results provide the first step in further understanding multisensory convergence in normal gravity, as this task is fundamental to our appreciation of neurovestibular adaptation to altered gravity.