Experiments were performed in standing subjects to determine whether low-threshold cutaneous and muscle afferents from mechanoreceptors in the human foot reflexly influence fusimotor neurons innervating pretibial flexor muscles. Recordings were made from 30 identified muscle-spindle afferents, four tendon-organ afferents, and one α-motor axon innervating the pretibial flexor muscles. The subjects stood without support or vision on a force platform while trains of electrical stimuli (5 stimuli, 300 Hz) were delivered at nonpainful intensities to the sural nerve or to the posterior tibial nerve at the ankle. Seventeen of the 30 spindle endings had no background discharge, and none was activated by the sural or posterior tibial stimuli. Five silent afferents were given a background discharge by sustained pressure on the relevant tendon, but with two the discharge was dominated by a tremor rhythm obscuring any reflex response to the stimuli. Based on peristimulus time histograms (PSTHs), the sural stimuli then produced increases in discharge of two of the remaining three endings at latencies of 84 and 90 ms. These effects could not be explained by muscle stretch and are presumed to have been fusimotor mediated. When the subjects stood freely without support or vision, 13 muscle-spindle endings had a background discharge, but with three endings tremor developed at the ankle and dominated the spindle discharge. Sural stimuli affected the discharge of five of nine endings unaffected by tremor. With three of these endings, there were changes in discharge that could be explained by muscle stretch. With the remaining two endings, there were increases in discharge at latencies of 80 and 108 ms, both of which were presumably fusimotor mediated. Posterior tibial stimuli altered the discharge of four of five endings unaffected by tremor. With three the change in spindle discharge could be explained by a change in muscle length (stretch with 2 afferents, shortening with 1). With one afferent an increase in discharge occurred at a latency of 104 ms, presumably through fusimotor mechanisms. When the basally active spindle endings (n = 13) and those activated by additional stretch (n = 5) were considered together, presumed fusimotor reflexes were demonstrated for five endings. However, entrainment to tremor precluded the demonstration of any fusimotor reflex with five endings. There were poststimulus changes in discharge that could have been due to stretch instead of, or in addition to, any fusimotor action with a further three endings. The above stimuli had reflex effects on α-motoneuron pools, as revealed by averaging the electromyogram (EMG) of tibialis anterior (TA), peroneus longus (PL), and soleus, while the subjects stood without support or vision. These reflex effects were readily demonstrable for each muscle in both surface and needle EMG recordings, but only when the relevant muscle had background activity. Recordings were obtained from a single α-motor axon innervating TA, identified by spike-triggered averaging of EMG. Stimuli to both sural and posterior tibial nerves produced a decrease in its discharge at ~40-50 ms, in advance of a parallel change in EMG. With four of the above spindle endings, the stimuli that produced an increase in spindle discharge produced no detectable reflex EMG activity in the receptor-bearing muscle. Because these changes in spindle discharge could not be explained mechanically, they are presumed to have resulted from activation of γ-motoneurons at lower threshold than α-motoneurons. The present results contrast with our previous inability to demonstrate reflex modulation of muscle-spindle discharge in the pretibial muscles of recumbent subjects, even when the muscles were contracted to ensure that the spindle endings were under background fusimotor drive. The results are therefore consistent with task-dependent gating of reflexes operating on fusimotor neurons.
