Integration of nonlabyrinthine inputs by the vestibular system: role in compensation following bilateral damage to the inner ear

Abstract

Inputs from the skin and muscles of the limbs and trunk as well as the viscera are relayed to the medial, inferior, and lateral vestibular nuclei. Vestibular nucleus neurons very quickly regain spontaneous activity following a bilateral vestibular neurectomy, presumably due to the presence of such nonlabyrinthine inputs. The firing of a small fraction of vestibular nucleus neurons in animals lacking labyrinthine inputs can be modulated by whole-body tilts; these responses are eliminated by a spinal transection, showing that they are predominantly elicited by inputs from the trunk and limbs. The ability to adjust blood distribution in the body and maintain stable blood pressure during movement is diminished following a bilateral vestibular neurectomy, but compensation occurs within a week. However, bilateral lesions of the caudal portions of the vestibular nuclei produce severe and long-lasting cardiovascular disturbances during postural alterations, suggesting that the presence of nonlabyrinthine signals to the vestibular nuclei is essential for compensation of posturally-related autonomic responses to occur. Despite these observations, the functional significance of nonlabyrinthine inputs to the central vestibular system remains unclear, either in modulating the processing of vestibular inputs or compensating for their loss.

Fig. 1

Matrix showing the convergence of limb inputs onto vestibular nucleus neurons. The shading of each pair of boxes indicates whether a unit responded to stimulation of forelimb (F) or hindlimb (H) nerves containing muscle afferents. Different shading patterns designate whether the unit's firing was affected by low current intensities that only activated large afferents from muscle spindles and Golgi tendon organs or higher intensities that also stimulated small afferents. The top panel shows findings from animals that had previously sustained a bilateral vestibular neurectomy, whereas the bottom panel provides information from labyrinth-intact animals. Data are from [13].

Fig. 2

The rate and coefficient of variation (CV) of spontaneous activity of vestibular nucleus neurons before and in the first week following removal of vestibular inputs through a bilateral vestibular neurectomy. Data were collected from two animals that were conscious during recordings, as described in [16].

Fig. 3

Characteristics of vestibular nucleus neuronal responses to vertical rotations following the removal of labyrinthine inputs. Data were collected either from conscious animals or decerebrate cats that sustained a bilateral vestibular neurectomy approximately two months before the acute recording session. A: Bode plots indicating the response dynamics of neurons in animals lacking labyrinthine inputs. Response gain and phase are plotted with respect to stimulus position. B: Polar plot showing the response vector orientations of vestibular nucleus neurons following a bilateral vestibular neurectomy. Numbers along the radius of the plot indicate gain (spikes/s/°). Abbreviations: CED, contralateral ear down roll; IED, ipsilateral ear down roll; ND, nose down pitch; NU, nose up pitch. Data are from [16, 32].

Fig. 4

Responses to rotations in vertical planes of a neuron in the caudal fastigial nucleus of a conscious cat that had sustained a bilateral vestibular neurectomy. A: Examples of responses to sinusoidal pitch tilts at three different frequencies; the response vector orientation of the neuron was only 6° from the pitch plane, and its activity increased during head-up tilts. The amplitudes of rotations were 15° at 0.05 and 0.1 Hz and 10° at 0.5 Hz. The number of sweeps averaged to generate each trace are as follow: 0.05 and 0.1 Hz, 10; 0.5 Hz, 50. B: Bode plot indicating the response dynamics of the neuron; response gain and phase are plotted relative to stimulus position.

Fig. 5

Changes in arterial blood pressure recorded in conscious cats during 60° head-up tilts subsequent to peripheral or central vestibular system lesions. Each panel shows averaged data from a single animal. To simplify comparisons, the blood pressure changes were plotted relative to those that occurred before lesions. Responses recorded in the first week following lesions are depicted by dashed lines, and those determined during the subsequent three weeks are indicated by solid lines. Error bars represent one standard error. A: responses recorded following a bilateral vestibular neurectomy; data are from [12]. B: responses recorded following a combined ablation of the cerebellar uvula and a bilateral vestibular neurectomy; data are from [10]. C: responses recorded following placing chemical lesions bilaterally in the caudal vestibular nuclei; data are from [18].