Responses of caudal vestibular nucleus neurons of conscious cats to rotations in vertical planes, before and after a bilateral vestibular neurectomy

Abstract

Although many previous experiments have considered the responses of vestibular nucleus neurons to rotations and translations of the head, little data are available regarding cells in the caudalmost portions of the vestibular nuclei (CVN), which mediate vestibulo-autonomic responses among other functions. This study examined the responses of CVN neurons of conscious cats to rotations in vertical planes, both before and after a bilateral vestibular neurectomy. None of the units included in the data sample had eye movement-related activity. In labyrinth-intact animals, some CVN neurons (22%) exhibited graviceptive responses consistent with inputs from otolith organs, but most (55%) had dynamic responses with phases synchronized with stimulus velocity. Furthermore, the large majority of CVN neurons had response vector orientations that were aligned either near the roll or vertical canal planes, and only 18% of cells were preferentially activated by pitch rotations. Sustained head-up rotations of the body provide challenges to the cardiovascular system and breathing, and thus the response dynamics of the large majority of CVN neurons were dissimilar to those of posturally-related autonomic reflexes. These data suggest that vestibular influences on autonomic control mediated by the CVN are more complex than previously envisioned, and likely involve considerable processing and integration of signals by brainstem regions involved in cardiovascular and respiratory regulation. Following a bilateral vestibular neurectomy, CVN neurons regained spontaneous activity within 24 h, and a very few neurons (<10%) responded to vertical tilts <15° in amplitude. These findings indicate that nonlabyrinthine inputs are likely important in sustaining the activity of CVN neurons; thus, these inputs may play a role in functional recovery following peripheral vestibular lesions.

Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs

“…One explanation for the reduced RVLM neuronal activity after the elimination of labyrinthine inputs is a loss of excitatory monosynaptic and polysynaptic excitatory drive to RVLM neurons from the vestibular nuclei. A caveat, however, is that a previous experiment showed that the average firing rate of spontaneously active neurons in the vestibular nuclei returned to prelesion levels within a day after bilateral transection of the VIIIth nerves (33), although this study did not address whether the activity of the subset of neurons that contribute to autonomic regulation was restored. Another possibility is that loss of labyrinthine inputs elicits a compensatory increase in the gain of the baroreceptor reflex, which fits with observations that instability in blood pressure during postural alterations dissipates within a week following a loss of labyrinthine inputs and vestibulo-sympathetic responses (31).…”

“…Data were collected from four conscious female purpose-bred adult cats (Liberty Research, Waverly, NY) that were instrumented using methods described in previous studies (18,33,34) for single-unit recordings. Animals were spayed by a veterinarian prior to being included in this study to prevent cyclic changes in hormonal levels that could have affected cardiovascular regulation.…”

“…Animals were spayed by a veterinarian prior to being included in this study to prevent cyclic changes in hormonal levels that could have affected cardiovascular regulation. In addition, surgical procedures were only conducted on animals that were highly tractable and that were gradually acclimated over a 1-to 2-mo period for 90 min of restraint during recording sessions (18,33,34).…”

“…Two surgical procedures were performed aseptically in a dedicated operating suite, as described in detail in prior publications (18,33,34). During each surgery, animals were initially anesthetized using an intramuscular injection of ketamine (20 mg/kg) and acepromazine (0.2 mg/kg), an endotracheal tube was inserted, and anesthesia was maintained using 1-2% isoflurane vaporized in O 2.…”

Effects of postural changes and removal of vestibular inputs on blood flow to and from the hindlimb of conscious felines

“…However, other inputs likely also participate, explaining why deficits in hindlimb vasoconstriction dissipate over time following vestibular lesions. There is evidence that inputs from muscle proprioceptors and cutaneous mechanoreceptors are processed along with signals from the inner ear by vestibular nucleus neurons and that these nonlabyrinthine inputs are amplified after vestibular lesions to permit a determination of body position in space (18,33). Mechanoreceptors in the walls of limb veins could provide signals to the central nervous system reflecting blood pooling during postural alterations (5,17).…”