Sustained Firing of Alpha and Gamma Hind Limb Motoneurons Induced by Stimulation of the Pudendal Nerve

Abstract

oz-Martínez. Sustained firing of alpha and gamma hind limb motoneurons induced by stimulation of the pudendal nerve. J Neurophysiol 88: 3232-3242, 2002; 10.1152/jn.00157.2002. Axons from receptors in the cat vaginal wall run in the sensory pudendal nerve (SPN), and brief (Ͻ10 s) vaginal probing (VP) in the decerebrate cat produces a long-lasting (Ͼ1 min) contraction of the triceps surae (TS) muscles. The aim of the present project was to find out whether brief SPN stimulation also produces sustained TS response and, eventually, to study the mechanisms involved in it. Decerebrate female cats were used. In some cats, TS electromyography (EMG) and tension response were recorded; stimulation of left SPN with single or repetitive trains of shocks produced a bilateral TS response that outlasted the stimulus Ͼ1 min as VP did. In paralyzed cats (pancuronium; Panc), intracellular recordings were made from hind limb motoneurons (MNs). SPN stimulation produced a depolarization Յ5 s long and occasional cell firing only lasting Ͻ2.5 s; this is in contrast with the prolonged TS postdischarge seen in nonparalyzed cats. If MNs were depolarized below the firing threshold by current injection, about half of them showed bistable firing that could last several minutes in response to SPN train. It is suggested that MNs might hyperpolarize after Panc injection. Before Panc injection, SPN train produced long-lasting (Ͼ1 min) electroneurographic (ENG) postdischarge in a small filament of the medial gastrocnemius (MG) nerve; the MG EMG postdischarge was also recorded. Large spikes (LS) and small spikes (SS) were distinguished in the ENG. During the postdischarge, LS frequency and the integrated EMG activity correlated well (r Ͼ 0.9); no correlation was found between SS and EMG. After Panc injection, LS postdischarge was absent but the SS postdischarge remained. LS followed by EMG potential were also evoked by brief TS stretch (reflex LS); single shocks to SPN only elicited SS that were not followed by EMG potential. It is concluded that alpha axons and gamma axons produced LS and SS, respectively, and that SPN activates gamma axons. It is proposed that, in the nonparalyzed cats, the stimulation of SPN with trains of shocks might cause an increase in the afferent inflow from muscle spindles to alpha MNs through the sustained firing of gamma MNs. The increased excitatory inflow would depolarize alpha MNs and allow bistable MN firing; Panc would decrease this inflow by blocking transmission to the spindle fibers.

Gamma→Alpha Linkage and Persistent Firing of Ia Fibers by Pudendal Nerve Stimulation in the Decerebrate Cat

“…As previously shown, 100-to 200-ms-long trains of stimulation to SPN triggered a TS muscle response that outlasted the stimulus for several seconds (Cueva-Rolón et al 2002; see also Cueva-Rolón et al 1993); the stimulus also induced a sustained increase in the firing rate of Ia spikes (n ϭ 12). The onset of this increase always preceded the muscle response and outlasted it (Fig.…”

“…(Cueva-Rolón et al 2002). This mode of firing, however, was only obtained by depolarizing the MN membrane 2-3 mV below the firing threshold before the SPN was stimulated; at the resting membrane potential, bistable MN firing could not be obtained (Cueva-Rolón et al 2002; see also Paroschy and Shefchyk 2000). In fact, membrane depolarization below the firing threshold is a condition for the MNs to show bistability (Hounsgaard et al 1984).…”

“…Stimulation of this nerve branch with trains of shocks reproduces the motor effects of VP, and in cats that were paralyzed by a curarizing agent, bistable MN firing was elicited. (Cueva-Rolón et al 2002). This mode of firing, however, was only obtained by depolarizing the MN membrane 2-3 mV below the firing threshold before the SPN was stimulated; at the resting membrane potential, bistable MN firing could not be obtained (Cueva-Rolón et al 2002; see also Paroschy and Shefchyk 2000).…”

“…In fact, membrane depolarization below the firing threshold is a condition for the MNs to show bistability (Hounsgaard et al 1984). It was proposed that in paralyzed cats the MNs membrane potential might be below the voltage needed for bistability (Cueva-Rolón et al 2002).…”

“…In nonparalyzed cats, SPN stimulation induced a sustained postdischarge of axon spikes from both alpha-motoneurons (␣-MNs) and gamma-motoneurons (␥-MNs) to the medial gastrocnemious muscles (Cueva-Rolón et al 2002); the response of ␥ spikes outlasted that of ␣ spikes. Thus the prolonged firing of ␥ MNs might induce an equally prolonged discharge of primary muscle spindle afferents that could induce the depolarization of ␣ MNs that is needed for bistability.…”