The Role of the Vestibular Nucleus in the Multimodal Coordination of Balance

Abstract

Balance is a complex neurological process that makes use of multimodal sensory information. Regulation of balance relies on the integration of sensory information about the body's position and acceleration relative to gravity (vestibular inputs, provided by organs in the inner ears) with information about the body's position relative to itself (proprioceptive inputs, provided by receptors in joints and muscles). In addition, vestibular reflexes can be modified by feedback from the limbs. However, the neural populations and mechanisms underlying multimodal balance control remain to be determined. We hypothesized that neurons in the vestibular nuclei (VN) participate in multimodal balance control by integrating vestibular and proprioceptive sensory information. To test this hypothesis, we recorded activity from single VN neurons in decerebrate and conscious cats, and determined whether they responded to movement of the limb (to activate proprioceptors) and whole body (to activate vestibular receptors). Hindlimb extension‐flexion (movement of the limb in the rostral‐caudal plane) stimuli were generated via a limb‐attached motor, and vestibular stimuli were generated using a hydraulic table. In the decerebrate preparation, 70 neurons histologically demonstrated to be in the VN exhibited a response to hindlimb stimulation. These responses were classified on the basis of cell activity changes during each of four movements (midline‐to‐extension, extension‐to‐midline, midline‐to‐flexion, and flexion‐to‐midline). Most (81.4%, 57/70) of these neurons encoded information about the direction of limb movement, while the others responded similarly to movement in any direction. Of 51 of these neurons tested for a vestibular response, 56.9% (29/51) demonstrated a significant response (signal‐to‐noise ratio> 0.5). In conscious animals, vestibular stimulation was used as a search stimulus to localize VN neurons. Two‐thirds (67.7%, 65/96) of the VN cells whose activity was modulated by vestibular stimulation had a significant response to hindlimb stimulation. Only 41.5% (27/65) of these neurons encoded the direction of the leg stimulation in their responses. These results demonstrate the convergence of vestibular and somatosensory information onto individual VN neurons. However, the responses of VN neurons to hindlimb movement differed in the conscious and decerebrate preparations: responses in decerebrate preparations were much more likely to encode the direction of limb movement (p<0.001, Fisher's exact test). This indicates the presence of cortical modulation of these responses. Our future work will delve further into the role of higher brain centers in modulating the responses of VN neurons to vestibular and proprioceptive inputs.