Contributions of skin and muscle afferent input to movement sense in the human hand

Abstract

In the stationary hand, static joint-position sense originates from multimodal somatosensory input (e.g., joint, skin, and muscle). In the moving hand, however, it is uncertain how movement sense arises from these different submodalities of proprioceptors. In contrast to static-position sense, movement sense includes multiple parameters such as motion detection, direction, joint angle, and velocity. Because movement sense is both multimodal and multiparametric, it is not known how different movement parameters are represented by different afferent submodalities. In theory, each submodality could redundantly represent all movement parameters, or, alternatively, different afferent submodalities could be tuned to distinctly different movement parameters. The study described in this paper investigated how skin input and muscle input each contributes to movement sense of the hand, in particular, to the movement parameters dynamic position and velocity. Healthy adult subjects were instructed to indicate with the left hand when they sensed the unseen fingers of the right hand being passively flexed at the metacarpophalangeal (MCP) joint through a previously learned target angle. The experimental approach was to suppress input from skin and/or muscle: skin input by anesthetizing the hand, and muscle input by unexpectedly extending the wrist to prevent MCP flexion from stretching the finger extensor muscle. Input from joint afferents was assumed not to play a significant role because the task was carried out with the MCP joints near their neutral positions. We found that, during passive finger movement near the neutral position in healthy adult humans, both skin and muscle receptors contribute to movement sense but qualitatively differently. Whereas skin input contributes to both dynamic position and velocity sense, muscle input may contribute only to velocity sense.

Fig. 1.

Experimental setup. A: top-down view with the subject sitting at the limb-motion device. Two motors apply movement independently to the hand, one at the wrist (green) and the other at the fingers (red). Two sphygmomometer cuffs are applied to the right forearm and a contact device to the left thumb and index finger. An opaque shield (vertical black bar) prevented the subject from seeing the right arm. A computer monitor provided visual feedback. B: graphical presentation of constant error (CE) at 3 points during a trial; red line denotes the MCP starting position, blue line denotes the target angle, and yellow line denotes the metacarpophalangeal (MCP) angle at which the subject indicated target arrival, in this example resulting in a small overshoot. The distance from the red line to the blue line is equivalent to 12 degrees of MCP flexion.

Fig. 2.

Wrist extension minimizes stretch of the finger extensor muscle during MCP flexion. MCP torque, MCP angle, wrist angle, instantaneous frequency (Inst Freq) of muscle spindle firing, and the raw neurogram (N. Radial) are shown in A and B, top to bottom. A: wrist movement did not occur, and the muscle spindle Ia afferent fired briskly in response to MCP flexion (black box). B: wrist extension reduced the afferent response to MCP flexion to just a few impulses (black box).

Fig. 3.

Hand anesthesia and/or wrist extension affected performance of the movement task. Representative single-trial data are shown from a representative subject. Interventional conditions were no intervention (A), hand anesthesia only (B), wrist extension only (C), and wrist extension and hand anesthesia (i.e., both interventions) (D). In B and C, the indicator movement (Contact) was delayed; in D, the subject was unaware of the MCP movement and so did not respond. Note the decrease in MCP torque resulting from wrist extension (shaded regions in C and D).

Fig. 4.

Data from a single subject, exemplifying the different effects from the 2 interventions. A: in the unanesthetized hand, wrist extension increased the slope of the CE vs. MCP velocity relationship without affecting average CE or variable error (VE). Open and filled circles represent average CE. B: hand anesthesia increased the slope of the CE vs. MCP velocity relationship while also increasing the average CE or VE. ○, average CE; ●, single trial CE.

Fig. 5.

Awareness of MCP motion depended on velocity when the 2 interventions were combined. Averaged data from the 9 enrolled subjects showed that, for 8 degree/s MCP rotations, subjects were unaware of the movement 70% of the time, whereas for 20 degrees/s, they were unaware of the movement 40% of the time.

Fig. 6.

Summary results for all subjects. Wrist extension had no effect on CE, whereas hand anesthesia increased CE relative to the no-intervention condition (leftmost 3 bars). Wrist extension had no effect on VE, whereas hand anesthesia increased VE relative to the no-intervention condition (middle 3 bars). Both wrist extension and hand anesthesia interventions increased the slope of the CE vs. MCP velocity relationship relative to the no-intervention condition (rightmost 3 bars). Significance, *P ≤ 0.05, **P ≤ 0.001, ***P < 0.0001.