Vestibular nucleus neurons respond to hindlimb movement in the decerebrate cat

Abstract

The vestibular nuclei integrate information from vestibular and proprioceptive afferents, which presumably facilitates the maintenance of stable balance and posture. However, little is currently known about the processing of sensory signals from the limbs by vestibular nucleus neurons. This study tested the hypothesis that limb movement is encoded by vestibular nucleus neurons and described the changes in activity of these neurons elicited by limb extension and flexion. In decerebrate cats, we recorded the activity of 70 vestibular nucleus neurons whose activity was modulated by limb movements. Most of these neurons (57/70, 81.4%) encoded information about the direction of hindlimb movement, while the remaining neurons (13/70, 18.6%) encoded the presence of hindlimb movement without signaling the direction of movement. The activity of many vestibular nucleus neurons that responded to limb movement was also modulated by rotating the animal's body in vertical planes, suggesting that the neurons integrated hindlimb and labyrinthine inputs. Neurons whose firing rate increased during ipsilateral ear-down roll rotations tended to be excited by hindlimb flexion, whereas neurons whose firing rate increased during contralateral ear-down tilts were excited by hindlimb extension. These observations suggest that there is a purposeful mapping of hindlimb inputs onto vestibular nucleus neurons, such that integration of hindlimb and labyrinthine inputs to the neurons is functionally relevant.

Keywords: balance; hindlimb; locomotion; multisensory integration; proprioceptor.

Fig. 1.

A: position of the hindlimb and the approximate angles of the knee and hip joints during the midline, extension, and flexion phases of the stimulus. B: method for determining responses of vestibular nucleus neurons to hindlimb movement. Neuronal firing is binned in 0.1-s intervals. The final second of the midline (neutral) position was taken as baseline (bracket from 4 to 5 s) and was used as the basis for comparison. The bin in the subsequent segment (ramp-and-hold movement from midline to flexion in this example) with the highest count was identified (arrow) and the surrounding bins (4 preceding and 5 following) were used as measures of peak firing in response to the hindlimb movement. Ramp velocity: 60°/s. M-F, midline to flexion interval (hindlimb movement to reposition the limb from the midline to flexion positions).

Fig. 2.

Vestibular nucleus neuronal firing rate is modulated by hindlimb movement. A: tracing showing that the firing rate of a vestibular nucleus neuron increased with hindlimb movement from midline to flexion. The firing rate of the neuron decreased in response to hindlimb movement to extension (hindlimb position tracing in B; neuronal data sampled at 25 kHz). C: average waveforms from this neuron were identical across all hindlimb positions indicating that the same neuron was recorded throughout the trial; average waveforms were generated from 159, 262, and 347 individual tracings for the extension, midline, and flexion segments, respectively. Ramp velocity: 15°/s.

Fig. 3.

Vestibular nucleus neurons exhibited one of four categories of responses to ramp-and-hold movements of the hindlimb: reciprocal (A), unidirectional (B), bidirectional (C), or omnidirectional (D). *Responses that met the criteria outlined in the methods section and Fig. 1. Bins are in 0.1-s intervals. Ramp speed: 60°/s.

Fig. 4.

Dynamics of responses of vestibular nucleus neurons to hindlimb motion. Response gains increased modestly as stimulus frequency was advanced. Response phases were between stimulus position and velocity. A: dynamics of responses of individual vestibular nucleus neurons to movement of the hindlimb at multiple frequencies. B: mean response dynamics. Bars indicate SE.

Fig. 5.

Sensitivity of vestibular nucleus neurons to sinusoidal hindlimb movements. A: sensitivity of individual vestibular nucleus neurons to movement of the hindlimb at multiple amplitudes. B: mean sensitivity increased to 1.4 ± 0.2 spikes·s⁻¹·deg⁻¹ when 7.5° sinusoidal movements were delivered from 0.5 ± 0.1 spikes·s⁻¹·deg⁻¹ when 60° sinusoidal movements were delivered. Movements were delivered at 0.5 Hz. Bars indicate SE.

Fig. 6.

Response vector orientations to vestibular stimulation in vertical planes for neurons with different types of responses to hindlimb movements. CED, contralateral ear down; IED, inpsilateral ear down; ND, nose down; NU, nose up.

Fig. 7.

Average dynamics of responses to whole body rotations of vestibular nucleus neurons whose activity was modulated by hindlimb motion. Bars indicate standard error.

Fig. 8.

Locations of neurons that were responsive to hindlimb movement in the inferior, medial, and lateral vestibular nuclei.