Representation of wrist joint kinematics by the ensemble of muscle spindles from synergistic muscles

Abstract

Proprioceptive information about movement is transmitted to the central nervous system by a variety of receptor types, which are widely distributed among the muscles, joints, and skin. Muscle spindles are known to be an important and reliable source of information for the perception of movement kinematics. Previous studies that focused on the characteristics of single muscle spindle firing patterns have left the impression that each receptor fires in relation to a number of kinematic variables, leaving the following question unanswered: what role is played by the ensemble of muscle spindles within the same muscle or within synergistic muscles? The study described in this paper addressed whether the perception of joint position and velocity is based on the net input of muscle spindles residing in all synergistic muscles crossing a joint. Normal human adults performed a motor coordination task that required perception of joint velocity and dynamic position at the wrist. The task was to open the left hand briskly as the right wrist was passively rotated in the flexion direction through a prescribed target angle. In randomly occurring trials, the tendons to three muscles [extensor carpi radialis (ECR), extensor carpi ulnaris (ECU), and extensor digitorum (ED)] were vibrated either individually or in different combinations during the performance of the motor task. Tendon vibration is known to distort muscle spindle firing patterns, and consequently, kinesthesia. By comparing performance errors with and without tendon vibration, the relative influences of muscle spindles residing in ECR, ECU, and ED were quantified. Vibration of the individual ECR, ECU, or ED tendons produced systematic undershoot errors in performance, consistent with the misperception of wrist velocity and dynamic position. Performance errors were larger when combinations of, rather than individual, muscle tendons were vibrated. The error resulting from simultaneous vibration of ECR and ECU was roughly equal to the sum of the errors produced by vibration of the individual tendons. These effects of vibrating synergistic tendons at the wrist suggest that kinesthesia is derived from the integrated input of muscle spindles from all synergistic muscles.