Muscle spindles are ubiquitous encapsulated mechanoreceptors found in most mammalian muscles. There are two types of endings, primary and secondary, and both are sensitive to changes in muscle length and velocity, with the primary endings having a greater dynamic sensitivity. Unlike other mechanoreceptors in the somatosensory system, muscle spindles are unique in possessing motor innervation, via γ-motoneurons (fusimotor neurons), that control their sensitivity to stretch. Much of what we know about human muscles spindles comes from studying the behavior of their afferents via intraneural microelectrodes (microneurography) inserted into accessible peripheral nerves. We review the functional properties of human muscle spindles, comparing and contrasting with what we know about the functions of muscle spindles studied in experimental animals. As in the cat, many human muscle spindles possess a background discharge that is related to the degree of muscle stretch, but mean firing rates are much lower (~10 Hz). They can faithfully encode changes in muscle fascicle length in passive conditions, but higher level extraction of information is required by the central nervous system to measure changes in muscle length during muscle contraction. Moreover, although there is some evidence supporting independent control of human muscle spindles via fusimotor neurons, any effects are modest compared with the clearly independent control of fusimotor neurons observed in the cat.
We recently developed an approach for recording from muscle spindles in the intrinsic muscles of the foot in freestanding humans by inserting a tungsten microelectrode into the posterior tibial nerve behind the medial malleolus of the ankle. Here we characterize the behavior of muscle spindles in the small muscles of the foot in 1) seated subjects with the leg horizontal and the foot naturally plantarflexed and 2) standing subjects. In the first study, recordings were made from 26 muscle spindle afferents located within flexor digiti minimi brevis ( n = 4), abductor digiti minimi ( n = 3), quadratus plantae ( n = 3), plantar interossei ( n = 4), flexor digitorum brevis ( n = 3), dorsal interossei ( n = 2), and lumbricals ( n = 2), with one each supplying abductor hallucis, adductor hallucis, and flexor hallucis brevis. The identity of another two muscle afferents was unknown. The majority of the units were silent at rest, only seven (27%) being spontaneously active. Because of the anatomic constraints of the foot, some spindles supplying muscles acting on the toes responded to movements of one or more digits. In the second study, 12 muscle spindle afferents were examined during standing. The ongoing discharge of eight spindle afferents covaried with changes in the center of pressure during postural sway. We conclude that the majority of spindle endings in the small muscles of the foot are silent at rest, which may allow them to encode changes in conformation of the foot when it is loaded during standing. Moreover, these muscle spindle afferents can provide useful proprioceptive information during standing and postural sway. NEW & NOTEWORTHY We have characterized the firing properties of muscle spindles in the intrinsic muscles of the human foot for the first time. The majority of the spindle endings are silent in seated subjects, and most fire tonically during standing, their discharge covarying with center of pressure during postural sway. We conclude that spindle endings in the intrinsic muscles of the foot provide useful proprioceptive information during free standing.
The posterior tibial nerve, located behind the medial malleolus of the ankle, supplies the intrinsic muscles of the foot and most of the skin of the sole. We describe a novel approach for recording from this nerve via a percutaneously inserted tungsten microelectrode and provide examples of recordings from presumed muscle spindle endings recorded in freely standing human subjects. The fact that the angular excursions of the ankle joint are small as the foot is loaded during the transition from the seated position to standing means that one can obtain stable recordings of neural traffic in unloaded, loaded, and freely standing conditions. We conclude that this novel approach will allow studies that will increase our understanding of the roles of muscle and cutaneous afferents in the foot in the control of upright posture. NEW & NOTEWORTHY We have performed the first microneurographic studies from the posterior tibial nerve at the ankle. Stability of the recording site allows one to record from muscle spindles in the intrinsic muscles of the foot as well as from cutaneous mechanoreceptors in the sole of the foot during the transition from seated to standing. This novel approach opens up new opportunities for studying the roles of muscle and cutaneous afferents in the foot in the control of upright stance.
Knellwolf TP, Hammam E, Macefield VG. The vestibular system does not modulate fusimotor drive to muscle spindles in relaxed leg muscles of subjects in a near-vertical position.
We tested the hypothesis that random variations in the magnitude of sinusoidal linear acceleration cause greater modulation of skin sympathetic nerve activity (SSNA), but not muscle sympathetic nerve activity (MSNA), than sinusoidal stimuli of the same frequency but constant amplitude. Subjects (n = 22) were seated in a sealed room mounted on a linear motor that could deliver peak sinusoidal accelerations of 30 mG in the antero-posterior direction. Subjects sat on a padded chair with their neck and head supported vertically, thereby minimizing somatosensory cues, facing the direction of motion in the anterior direction. Each block of sinusoidal motion was delivered at 0.2 Hz, either with a constant-amplitude (root mean square 14 mG) or randomly fluctuating amplitudes of the same mean amplitude. MSNA (n = 12) and SSNA (n = 10) were recorded via tungsten microelectrodes inserted into muscle or cutaneous fascicles of the common peroneal nerve. Cross-correlation analysis was used to measure the magnitude of vestibular modulation. The modulation index for SSNA was significantly higher during delivery of random vs constant-amplitude acceleration (31.4 ± 1.9 vs 24.5 ± 2.5%), but there was no significant difference in the modulation indices for MSNA (28.8 ± 2.9 vs 33.4 ± 4.1%). We conclude that the pattern of vestibular stimulation affects the magnitude of modulation of sympathetic outflow to skin but not to muscle. Presumably, this is related to the subperceptual development of nausea, which is known to be associated with greater vestibular modulation of SSNA but not MSNA.
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