Research Article: Population Coding of Forelimb Joint Kinematics by Peripheral Afferents in Monkeys

Date Published: October 24, 2012

Publisher: Public Library of Science

Author(s): Tatsuya Umeda, Kazuhiko Seki, Masa-aki Sato, Yukio Nishimura, Mitsuo Kawato, Tadashi Isa, Paul L. Gribble.


Various peripheral receptors provide information concerning position and movement to the central nervous system to achieve complex and dexterous movements of forelimbs in primates. The response properties of single afferent receptors to movements at a single joint have been examined in detail, but the population coding of peripheral afferents remains poorly defined. In this study, we obtained multichannel recordings from dorsal root ganglion (DRG) neurons in cervical segments of monkeys. We applied the sparse linear regression (SLiR) algorithm to the recordings, which selects useful input signals to reconstruct movement kinematics. Multichannel recordings of peripheral afferents were performed by inserting multi-electrode arrays into the DRGs of lower cervical segments in two anesthetized monkeys. A total of 112 and 92 units were responsive to the passive joint movements or the skin stimulation with a painting brush in Monkey 1 and Monkey 2, respectively. Using the SLiR algorithm, we reconstructed the temporal changes of joint angle, angular velocity, and acceleration at the elbow, wrist, and finger joints from temporal firing patterns of the DRG neurons. By automatically selecting a subset of recorded units, the SLiR achieved superior generalization performance compared with a regularized linear regression algorithm. The SLiR selected not only putative muscle units that were responsive to only the passive movements, but also a number of putative cutaneous units responsive to the skin stimulation. These results suggested that an ensemble of peripheral primary afferents that contains both putative muscle and cutaneous units encode forelimb joint kinematics of non-human primates.

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Peripheral inputs contribute to kinesthesia, the sense of joint position and movements, and blocking peripheral primary afferents impairs the perception of limb position and movements [1], [2], [3], [4]. More directly, artificial activation of muscle tendons or surface cutaneous receptors induces a powerful illusion of movement [5], [6], [7], [8], [9]. Human studies have shown that peripheral deafferented patients showed error in hand movements without visual feedback [10], [11]. In monkeys that have had the dorsal root transected at the level of the cervical spinal cord, precision grip is severely impaired [12]. Thus, positional information arising from inputs of peripheral afferents is critical to achieve accurate and dexterous movements of the hands and arms of primates.

Two adult male monkeys (Macaca mulatta, body weight; 4.6 and 9.6 kg, respectively) were used in this study. The experiments were approved by the animal experimental committee of the National Institute of Natural Sciences (Approved Nos.: 09A196, 10A203, 11A168) and were performed in accordance with the Weatherall report, “The use of non-human primates in research”. Before the experiments, the animals were housed individually on a 12-hour light/dark cycle and provided a rubber toy. They were not food and water deprived.

Recordings were obtained from the DRGs at the C7 and C8 segments with two multi-electrode arrays. A total of 112 units (39 from C7, 73 from C8) were discriminated from 43 channels in Monkey 1 and 92 units (38 from C7, 54 from C8) were discriminated from 44 channels in Monkey 2.

The results of the present study demonstrate that temporal changes in angle, velocity, and acceleration of various forelimb joints can be reconstructed from the population activities recorded from cervical DRGs in monkeys using the SLiR. The analysis provided improved generalization performance in the reconstruction of various joint kinematics from a subset of somatosensory neural activity. The analysis elucidated that, not only the putative muscle units, but a number of the putative cutaneous units also contributed to reconstruction of joint kinematics. The result was confirmed by reconstruction of joint kinematics from activity of individual classes of units. The putative muscle units contributed greatly to encoding of elbow joint kinematics, but the putative cutaneous units provided additional information regarding the joint kinematics, especially at wrist and finger joints.