Effects of tonic muscle pain on fusimotor control of human muscle spindles during isometric ankle dorsiflexion

Studies on anesthetized animals have revealed that nociceptors can excite fusimotor neurons and thereby change the sensitivity of muscle spindles to stretch; such nociceptive reflexes have been suggested to underlie the mechanisms that lead to chronic musculoskeletal pain syndromes. However, the validity of the “vicious cycle” hypothesis in humans has yielded results contrasting with those found in animals. Given that spindle firing rates are much lower in humans than in animals, it is possible that some of the discrepancies between human experimental data and those obtained in animals could be explained by differences in background fusimotor drive when the leg muscles are relaxed. We examined the effects of tonic muscle pain during voluntary contractions of the ankle dorsiflexors. Unitary recordings were obtained from 10 fusimotor-driven muscle spindle afferents (6 primary, 4 secondary) supplying the ankle dorsiflexors via a microelectrode inserted percutaneously into the common peroneal nerve. A series of 1-min weak contractions was performed at rest and during 1 h of muscle pain induced by intramuscular infusion of 5% hypertonic saline into the tibialis anterior muscle. We did not observe any statistically significant increases in muscle spindle firing rates of six afferents followed during tonic muscle pain, although discharge variability increased slightly. Furthermore, a participant’s capacity to maintain a constant level of force, while relying on proprioceptive feedback in the absence of visual feedback, was not compromised during pain. We conclude that nociceptive inputs from contracting muscle do not excite fusimotor neurons during voluntary isometric contractions in humans. NEW & NOTEWORTHY Data obtained in the cat have shown that muscle pain causes a marked increase in the firing of muscle spindles, attributed to a nociceptor-driven fusimotor reflex. However, our studies of muscle spindles in relaxed leg muscles failed to find any effect on spindle discharge. Here we showed that experimental muscle pain failed to increase the firing of muscle spindle afferents during weak voluntary contractions, when fusimotor drive sufficient to increase their firing is present.

Firing properties of muscle spindles supplying the intrinsic foot muscles of humans in unloaded and freestanding conditions

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.

Two distinct proprioceptive representations of voluntary movements in primate spinal neurons

When willingly setting our body in motion, we simultaneously know where and how our limbs are moving. While this indicates that proprioceptive information is readily represented in the neurons of the central nervous system, it is still unclear how. We recorded the activity of spinal neurons with direct projections from muscle spindle afferents in four monkeys, while they performed simple wrist movements. Against the assumption that these spinal neurons act as a simple relay of afferent input, we found the majority (56%) of neurons had firing patterns incongruent with a simple representation of spindle activity, and the minority had congruent patterns. Two groups of neurons showed distinct intrinsic characteristics (spike width, base firing rate and firing irregularity), and distinct control of their input-output gain. These results are the first demonstration that proprioceptive representation is achieved by the coordinated activity of distinct groups of neurons during volitional movement.

Muscle spindles in human tibialis anterior encode muscle fascicle length changes

Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions, compliant structures can act to decouple the fascicles, and, therefore, the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1–0.5 Hz) and amplitudes (1–9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length, and spindle firing patterns. NEW & NOTEWORTHY Muscle spindles are exquisitely sensitive to changes in muscle length, but recordings from human muscle spindle afferents are usually correlated with joint angle rather than muscle fascicle length. In this study, we monitored both muscle fascicle length and spindle firing from the human tibialis anterior muscle in vivo. Our findings are the first to measure these signals in vivo and provide an experimental basis for exploring this link further.

Muscle spindle responses to horizontal support surface perturbation in the anesthetized cat: insights into the role of autogenic feedback in whole body postural control

Intact cats and humans respond to support surface perturbations with broadly tuned, directionally sensitive muscle activation. These muscle responses are further sensitive to initial stance widths (distance between feet) and perturbation velocity. The sensory origins driving these responses are not known, and conflicting hypotheses are prevalent in the literature. We hypothesize that the direction-, stance-width-, and velocity-sensitive muscle response during support surface perturbations is driven largely by rapid autogenic proprioceptive pathways. The primary objective of this study was to obtain direct evidence for our hypothesis by establishing that muscle spindle receptors in the intact limb can provide appropriate information to drive the muscle response to whole body postural perturbations. Our second objective was to determine if spindle recordings from the intact limb generate the heightened sensitivity to small perturbations that has been reported in isolated muscle experiments. Maintenance of this heightened sensitivity would indicate that muscle spindles are highly proficient at detecting even small disturbances, suggesting they can provide efficient feedback about changing postural conditions. We performed intraaxonal recordings from muscle spindles in anesthetized cats during horizontal, hindlimb perturbations. We indeed found that muscle spindle afferents in the intact limb generate broadly tuned but directionally sensitive activation patterns. These afferents were also sensitive to initial stance widths and perturbation velocities. Finally, we found that afferents in the intact limb have heightened sensitivity to small perturbations. We conclude that muscle spindle afferents provide an array of important information about biomechanics and perturbation characteristics highlighting their potential importance in generating appropriate muscular response during a postural disturbance.