title: Integration of canal and otolith inputs by central vestibular neurons is subadditive for both active and passive self-motion: implication for perception.
abstract: Traditionally, the neural encoding of vestibular information is studied by applying either passive rotations or translations in isolation. However, natural vestibular stimuli are typically more complex. During everyday life, our self-motion is generally not restricted to one dimension, but rather comprises both rotational and translational motion that will simultaneously stimulate receptors in the semicircular canals and otoliths. In addition, natural self-motion is the result of self-generated and externally generated movements. However, to date, it remains unknown how information about rotational and translational components of self-motion is integrated by vestibular pathways during active and/or passive motion. Accordingly, here, we compared the responses of neurons at the first central stage of vestibular processing to rotation, translation, and combined motion. Recordings were made in alert macaques from neurons in the vestibular nuclei involved in postural control and self-motion perception. In response to passive stimulation, neurons did not combine canal and otolith afferent information linearly. Instead, inputs were subadditively integrated with a weighting that was frequency dependent. Although canal inputs were more heavily weighted at low frequencies, the weighting of otolith input increased with frequency. In response to active stimulation, neuronal modulation was significantly attenuated (∼ 70%) relative to passive stimulation for rotations and translations and even more profoundly attenuated for combined motion due to subadditive input integration. Together, these findings provide insights into neural computations underlying the integration of semicircular canal and otolith inputs required for accurate posture and motor control, as well as perceptual stability, during everyday life.
authors.affiliation: Department of Physiology McGill University, Montreal, Quebec, Canada H3G 1Y6.
authors.forename: Jerome
authors.initials: J
authors.lastname: Carriot
authors.affiliation: Department of Physiology McGill University, Montreal, Quebec, Canada H3G 1Y6.
authors.forename: Mohsen
authors.initials: M
authors.lastname: Jamali
authors.affiliation: Department of Physiology McGill University, Montreal, Quebec, Canada H3G 1Y6.
authors.forename: Jessica X
authors.initials: JX
authors.lastname: Brooks
authors.affiliation: Department of Physiology McGill University, Montreal, Quebec, Canada H3G 1Y6 kathleen.cullen@mcgill.ca.
authors.forename: Kathleen E
authors.identifier: http://orcid.org/0000-0002-9348-0933
authors.initials: KE
authors.lastname: Cullen
mesh_terms: D000200:Action Potentials; D000818:Animals; D019416:Head Movements; D008253:Macaca mulatta; D008297:Male; D010037:Otolithic Membrane / Q000502:physiology*; D012665:Semicircular Canals / Q000502:physiology*; D011984:Sensory Receptor Cells / Q000502:physiology*; D013028:Space Perception; D014726:Vestibular Nuclei / Q000166:cytology / Q000502:physiology*
keywords: head motion; rotation; sensory integration; translation; vestibular nuclei; voluntary