Impulse rates and sensitivity to stretch of soleus muscle spindle afferent fibers during locomotion in premammillary cats

Abstract

Impulse from soleus muscle afferents were recorded in premammillary cats that were walking on a treadmill. In normal walking the effects of gamma-motoneurons on impulse rates of muscle spindle afferents are confounded by the effects of the large length changes that occur. To isolate the effects of gamma-motoneurons the leg was fixed in place for recording and denervated except for soleus muscle. Because gamma-motoneurons produce marked effects on the stretch sensitivity of muscle afferents, soleus muscle was oscillated about a present length so the stretch sensitivity of its afferents could be determined. The impulse rate of secondary muscle spindle afferents in soleus muscle was generally increased at all phases of the step cycle. The mean rate approximately doubled during walking (82 imp/s), compared with nonwalking (rest) periods (44 imp/s). The sensitivity to sinusoidal length changes was generally reduced throughout the step cycle (mean reduction = 33%). Primary muscle spindle afferents also showed an increased mean rate during walking (47 imp/s) compared with rest (24 imp/s). The impulse rate peaked after the muscle reached its maximum force and often showed a second peak before the maximum electromyogram (EMG) activity. The sensitivity to sinusoidal stretches varied cyclically during locomotion. During the extension phase it sometimes exceeded the resting value, but was greatly reduced during the flexion phase (mean reduction = 49% over whole cycle). Control experiments were carried out in which static and dynamic gamma-motoneurons were stimulated and activity from muscle spindle afferents was recorded in anesthetized cats. With the amplitude and frequency of stretch applied, stimulation of dynamic gamma-motoneurons usually increased and stimulation of static gamma-motoneurons usually decreased the sensitivity of primary muscle spindle afferents to sinusoidal stretch. The patterns observed in muscle spindle afferents suggest a strong, maintained activation of static gamma-motoneurons throughout the step cycle and a phasic activation of dynamic gamma-motoneurons, which is consistent with previous direct recordings from gamma-motoneurons. With this pattern of activating gamma-motoneurons, the secondary muscle spindle afferents will provide a good feedback signal of the large length changes that normally occur in the muscle during locomotion. The changes in sensitivity of primary muscle spindle afferents will complement central changes so the gain of the stretch reflex from extensors is high during extension (when required to help support the weight of the body) and low during flexion (when a high gain would be counterproductive).

Regulation of soleus muscle spindle sensitivity in decerebrate and spinal cats during postural and locomotor activities.

“…3B compared with 3A). Table 2 compares the averaged firing rates for these yd-drive (Yd,y8) in isolation (taken from Taylor et al 1985, scatter not shown but suggested by thick arrows). Dashed line: maximal modulation possible at a given rate (see Methods).…”

“…A possible contribution to this lowered stretch reflex is an increased activation of static y-motoneurones (static y-drive), which can reduce spindle sensitivity to stretch (Jansen & Matthews, 1962;Taylor, Stein & Murphy, 1985). Indeed, in decerebrate cats muscle spindle sensitivity is on average lower during locomotion compared with the pre-locomotor state, in spite of large increases in firing rates (Taylor et al 1985). Direct recordings from y-motoneurones in these cats support the idea that a strong static y-drive is initiated during locomotion (Murphy, Stein & Taylor, 1984;Bessou, Cabelguen, Joifroy, Montoya & Pags, 1986).…”

Reversal of fusimotor reflex responses during locomotion in the decerebrate cat

“…The present fusimotor classification has been described in detail elsewhere (Murphy et al 1984;Taylor et al 1985;Murphy & Hammond, 1991) and we will mainly concentrate on its generality in the present discussion. In previous experiments, we found two groups of y-efferents in the triceps surae nerve.…”

“…The present, predominantly inhibitory locomotor responses to plantar input contrast with the only prior investigation of the effect of peripheral afferents on identified y-efferents during walking (Murphy & Hammond, 1991 During a steady, standing posture, where the sole of the foot is the load-bearing surface, it is conceivable that an excitatory plantar reflex would be functionally useful in setting the level of static y-drive to ankle extensor muscles (anti-gravity), and the Ia support of extrafusal contraction. In contrast, during walking, a dynamic task in which plantar load varies (Manter, 1938;Grillner, 1972), a reversal of static y-reflexes to inhibition may be appropriate in contributing to the increase in I a afferent sensitivity (and stretch reflex) that occurs in the stance phase, when ankle extensors undergo a lengthening contraction (Taylor et al 1985;Yang, Stein & James, 1991). In addition, it is possible that plantar inhibitory reflexes, which were maximum at peak background y-rate, are involved in the production of tonic static y-drive to gastrocnemius spindle afferents during walking in the intact cat (Prochazka, 1989).…”

“…It has been suggested that this pattern of fusimotor discharge would be functionally advantageous for the locomotor task (Taylor et al 1985). Thus the resultant high I a afferent sensitivity during stance will enhance the stretch reflex and assist in supporting the body and propelling it upwards and forwards.…”