Sensorimotor control in the congenital absence of functional muscle spindles.

Hereditary sensory and autonomic neuropathy type III (HSAN III), also known as familial dysautonomia or Riley-Day syndrome, results from an autosomal recessive genetic mutation that causes a selective loss of specific sensory neurones, leading to greatly elevated pain and temperature thresholds, poor proprioception, marked ataxia and disturbances in blood pressure control. Stretch reflexes are absent throughout the body, which can be explained by the absence of functional muscle spindle afferents - assessed by intraneural microelectrodes inserted into peripheral nerves in the upper and lower limbs. This also explains the greatly compromised proprioception at the knee joint, as assessed by passive joint-angle matching. Moreover, there is a tight correlation between loss of proprioceptive acuity at the knee and the severity of gait impairment. Surprisingly, proprioception is normal at the elbow, suggesting that participants are relying more on sensory cues from the overlying skin; microelectrode recordings have shown that myelinated tactile afferents in the upper and lower limbs appear to be normal. Nevertheless, the lack of muscle spindles does affect sensorimotor control in the upper limb: in addition to poor performance in the finger-to-nose test, manual performance in the Purdue pegboard task is much worse than in age-matched healthy controls. Unlike those rare individuals with large-fibre sensory neuropathy, in which both muscle spindle and cutaneous afferents are absent, those with HSAN III present as a means of assessing sensorimotor control following the selective loss of muscle spindle afferents.

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.

Impaired sensorimotor control of the hand in congenital absence of functional muscle spindles.

Patients with hereditary sensory and autonomic neuropathy type III (HSAN III) exhibit marked ataxia, including gait disturbances. We recently showed that functional muscle spindle afferents in the leg, recorded via intraneural microelectrodes inserted into the peroneal nerve, are absent in HSAN III, although large-diameter cutaneous afferents are intact. Moreover, there is a tight correlation between loss of proprioceptive acuity at the knee and the severity of gait impairment. We tested the hypothesis that manual motor performance is also compromised in HSAN III, attributed to the predicted absence of muscle spindles in the intrinsic muscles of the hand. Manual performance in the Purdue pegboard task was assessed in 12 individuals with HSAN III and 11 age-matched healthy controls. The mean (±SD) pegboard score (number of pins inserted in 30 s) was 8.1 ± 1.9 and 8.6 ± 1.8 for the left and right hand, respectively, significantly lower than the scores for the controls (15.0 ± 1.3 and 16.0 ± 1.1; P < 0.0001). Performance was not improved after kinesiology tape was applied over the joints of the hand. In 5 patients we inserted a tungsten microelectrode into the ulnar nerve at the wrist. No spontaneous or stretch-evoked muscle afferent activity could be identified in any of the 11 fascicles supplying intrinsic muscles of the hand, whereas touch-evoked activity from low-threshold cutaneous mechanoreceptor afferents could readily be recorded from 4 cutaneous fascicles. We conclude that functional muscle spindles are absent in the short muscles of the hand and most likely absent in the long finger flexors and extensors, and that this largely accounts for the poor manual motor performance in HSAN III. NEW & NOTEWORTHY We describe the impaired manual motor performance in patients with hereditary sensory and autonomic neuropathy type III (Riley-Day syndrome), who exhibit congenital insensitivity to pain, poor proprioception, and marked gait ataxia. We show that functional muscle spindles are absent in the intrinsic muscles of the hand, which we argue contributes to their poor performance in a task involving the precision grip.