Responses of Renshaw cells coupled with hindlimb extensor motoneurons to sinusoidal stimulation of labyrinth receptors in the decerebrate cat

Abstract

• 1. Contraction of ipsilateral limb extensors during side-down roll tilt of the head, leading to selective stimulation of labyrinth receptors, is attributed to an increased discharge of excitatory vestibulospinal (VS) neurons (α-responses) and a decreased discharge of medullary inhibitory reticulospinal (RS) neurons (β-responses), both of which act on ipsilateral extensor motoneurons.

• 2. Experiments were performed in decerebrate cats, with the de-efferented gastrocnemius-soleus (GS) muscle fixed at a constant length, to find out whether Renshaw (R) cells linked with GS motoneurons responded to labyrinth stimulation elicited by head rotation, while the neck had been bilaterally deafferented. We hoped in this way to clarify the role and the mechanism by which these inhibitory interneurons act on limb extensor motoneurons during the vestibular reflexes.

• 3. 72.7% of the R-cells, disynaptically excited by group I volleys elicited by single shock stimulation of the GS nerve, weakly responded to head rotation at frequencies of 0.026–0.15 Hz and at a peak amplitude of 10°.

• 4. For the frequency of head rotation of 0.026 Hz, ±10°C, most of the GS R-cells increased their firing rate during side-down head displacement (α-responses); some responses were related to head position, but others showed some phase lead or lag with respect to head position. The gain of the first harmonic of these unit responses was very low and corresponded on the average to 0.084±0.062, S.D. imp./s/deg, while the sensitivity corresponded to 2.14±2.35, S.D.%/deg (base frequency, 6.85±5.97, S.D.imp./s). These responses were attributed to the activity of VS neurons, the increased discharge of which during side-down head rotation exerts a weak excitatory influence on a limited number of GS motoneurons and, through their recurrent collaterals, on the related R-cells.

• 5. The modulation of the firing rate of R-cells coupled with the GS motoneurons increased linearly by increasing the peak amplitude of displacement from 5° to 20° at the frequency of 0.026 Hz, so that the response gain remained almost unchanged.

• 6. An increase in frequency of head rotation from 0.026 to 0.32 Hz at a fixed amplitude of 10°, thus changing the maximal angular acceleration from 0.26°/s² to 41.7°/s², reversed the response pattern of R-cells reported above. The resulting β-responses, which also showed some phase lead or lag with respect to head position, were attributed to vestibular activation of RS neurons. These neurons may directly excite the R-cells linked with the GS motoneurons, so that their reduced discharge during side-down head rotation would lead to a decrease in firing rate of the corresponding inhibitory interneurons. Interestingly, the response gain and sensitivity of these R-cells first decreased but then increased after reversal of the response pattern, by increasing frequency of head rotation. The critical frequency at which a cancellation of the response occurred before the response pattern was reversed, ranged between 0.051 and 0.15 Hz.

• 7. In conclusion, R-cells linked with the GS motoneurons displayed an α-pattern of response during low frequency head rotation, suggesting that they were largely activated by the recurrent collaterals of the corresponding motoneurons driven by the VS volleys. The same R-cells, however, exhibited the opposite β-pattern of response at higher stimulus frequencies, thus behaving as if they were decoupled from their input motoneurons and controlled more directly by the medullary RS neurons. In these instances, activation of GS motoneurons during side-down head rotation could be attributed not only to an increased discharge of the excitatory VS neurons, but also to a reduced discharge of the R-cells driven by the medullary RS neurons. This system may thus contribute to the gain regulation of the EMG responses of hindlimb extensors to labyrinth stimulation.