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.