Responses of vestibular nucleus neurons to tilt following chronic bilateral removal of vestibular inputs

Abstract

Recordings were made from the vestibular nuclei of decerebrate cats that had undergone a combined bilateral labyrinthectomy and vestibular neurectomy 49-103 days previously and allowed to recover. Responses of neurons were recorded to tilts in multiple vertical planes at frequencies ranging from 0.05 to 1 Hz and amplitudes up to 15 degrees. Many spontaneously active neurons were present in the vestibular nuclei; the mean firing rate of these cells was 43 +/- 5 (SEM) spikes/s. The spontaneous firing of the neurons was irregular: the coefficient of variation was 0.86 +/- 0.14. The firing of 27% of the neurons was modulated by tilt. The plane of tilt that elicited the maximal response was typically within 25 degrees of pitch. The response gain was approximately 1 spikes/s/degree across stimulus frequencies. The response phase was near stimulus position at low frequencies, and lagged position slightly at higher frequencies (average of 35 +/- 9 degrees at 0.5 Hz). The source of the inputs eliciting modulation of vestibular nucleus activity during tilt in animals lacking vestibular inputs is unknown, but could include receptors in the trunk or limbs. These findings show that activation of vestibular nucleus neurons during vertical rotations is not exclusively the result of labyrinthine inputs, and suggest that limb and trunk inputs may play an important role in graviception and modulating vestibular-elicited reflexes.

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

“…The present data support the findings of a previous study conducted in decerebrate cats that had undergone a bilateral vestibular neurectomy, which also showed that the firing of a small percentage of CVN neurons is altered by vertical tilts following the elimination of vestibular inputs (Yates et al 2000). In both decerebrate and conscious animals lacking labyrinthine inputs, most CVN neurons whose activity was modulated by vertical rotations were preferentially activated by pitch tilts, despite the fact that few units in this region responded best to pitch rotations in labyrinth-intact cats.…”

“…Our procedures for performing vertical vestibular simulation have been described in detail previously (e.g., Yates et al 2000;Jian et al 2002). We first determined the plane of tilt that produced maximal modulation of the unit's firing rate (response vector orientation).…”

“…In another experiment, recordings were made from CVN neurons of decerebrate cats that had recovered from a bilateral vestibular neurectomy performed 49-103 days previously. Curiously, approximately one-fourth of the units responded to rotations in the pitch plane despite an absence of labyrinthine inputs (Yates et al 2000), presumably as a consequence of nonlabyrinthine signals to the CVN that were altered in accordance with body position in space. It has been postulated that such "sensory substitution" in the CVN explains why posturally-related disturbances in blood pressure and respiration following a bilateral labyrinthectomy dissipate over time (Yates and Bronstein 2005).…”

Recovery of Gaze Stability During Vestibular Regeneration

“…Although very few studies have examined central recovery mechanisms following complete bilateral vestibular loss (similar to the types of lesions produced in the present study), it has been shown that central vestibular cells can recover some responsiveness to motion. The recovery is likely due to increased sensitivity to extra-vestibular cues such as vision, proprioception, somatosensory, and visceral receptors (Heimbrand et al 1996;Jensen 1979;Mittelstaedt 1992;Yates et al 2000). In animals that demonstrate spontaneous regeneration, a more complicated interplay is certainly involved, where a coupling occurs between immediate neural plasticity and the gradual return of dynamic vestibular receptor signals over a prolonged time.…”

“…Stage 1 regeneration lasted through the first month PST and was characterized by the exclusive low-density development of type II hair cells and bouton afferents (Masetto and Correia 1997a,b;Zakir and Dickman 2006). During this time, it is likely that increased sensitivity in central vestibular neurons to head/neck proprioceptive and somatosensory signals occurred through adaptive plasticity (Yates et al 2000). Plasticity, combined with the limited regenerating vestibular afferent signals was sufficient to elicit some recovery in the head component of gaze because closed feedback mechanisms were now being provided to the VCR and CCR.…”