Integration of vestibular and hindlimb inputs by vestibular nucleus neurons: multisensory influences on postural control

• Published in: Journal of neurophysiology Vol. 125; no. 4; pp. 1095 - 1110
• Main Authors: McCall, Andrew A, Miller, Derek M, Balaban, Carey D
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01.04.2021
• Series: Sensory Processing
• Subjects: Afferent Pathways; Animals; Behavior, Animal - physiology; Cats; Electrophysiological Phenomena - physiology; Female; Hindlimb - physiology; Movement - physiology; Neurons - physiology; Physical Stimulation; Postural Balance - physiology; Proprioception - physiology; Vestibular Nuclei - physiology; Vestibule, Labyrinth - physiology; limb; sensory integration; vestibular
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00350.2019

We recently demonstrated in decerebrate and conscious cat preparations that hindlimb somatosensory inputs converge with vestibular afferent input onto neurons in multiple central nervous system (CNS) locations that participate in balance control. Although it is known that head position and limb state modulate postural reflexes, presumably through vestibulospinal and reticulospinal pathways, the combined influence of the two inputs on the activity of neurons in these brainstem regions is unknown. In the present study, we evaluated the responses of vestibular nucleus (VN) neurons to vestibular and hindlimb stimuli delivered separately and together in conscious cats. We hypothesized that VN neuronal firing during activation of vestibular and limb proprioceptive inputs would be well fit by an additive model. Extracellular single-unit recordings were obtained from VN neurons. Sinusoidal whole body rotation in the roll plane was used as the search stimulus. Units responding to the search stimulus were tested for their responses to 10° ramp-and-hold roll body rotation, 60° extension hindlimb movement, and both movements delivered simultaneously. Composite response histograms were fit by a model of low- and high-pass filtered limb and body position signals using least squares nonlinear regression. We found that VN neuronal activity during combined vestibular and hindlimb proprioceptive stimulation in the conscious cat is well fit by a simple additive model for signals with similar temporal dynamics. The mean value for goodness of fit across all units was 0.74 ± 0.17. It is likely that VN neurons that exhibit these integrative properties participate in adjusting vestibulospinal outflow in response to limb state. Vestibular nucleus neurons receive convergent information from hindlimb somatosensory inputs and vestibular inputs. In this study, extracellular single-unit recordings of vestibular nucleus neurons during conditions of passively applied limb movement, passive whole body rotations, and combined stimulation were well fit by an additive model. The integration of hindlimb somatosensory inputs with vestibular inputs at the first stage of vestibular processing suggests that vestibular nucleus neurons account for limb position in determining vestibulospinal responses to postural perturbations.