Control of wrist position and muscle relaxation by shifting spatial frames of reference for motoneuronal recruitment: possible involvement of corticospinal pathways

Abstract

It has previously been established that muscles become active in response to deviations from a threshold (referent) position of the body or its segments, and that intentional motor actions result from central shifts in the referent position. We tested the hypothesis that corticospinal pathways are involved in threshold position control during intentional changes in the wrist position in humans. Subjects moved the wrist from an initial extended to a final flexed position (and vice versa). Passive wrist muscle forces were compensated with a torque motor such that wrist muscle activity was equalized at the two positions. It appeared that motoneuronal excitability tested by brief muscle stretches was also similar at these positions. Responses to mechanical perturbations before and after movement showed that the wrist threshold position was reset when voluntary changes in the joint angle were made. Although the excitability of motoneurons was similar at the two positions, the same transcranial magnetic stimulus (TMS) elicited a wrist extensor jerk in the extension position and a flexor jerk in the flexion position. Extensor motor-evoked potentials (MEPs) elicited by TMS at the wrist extension position were substantially bigger compared to those at the flexion position and vice versa for flexor MEPs. MEPs were substantially reduced when subjects fully relaxed wrist muscles and the wrist was held passively in each position. Results suggest that the corticospinal pathway, possibly with other descending pathways, participates in threshold position control, a process that pre-determines the spatial frame of reference in which the neuromuscular periphery is constrained to work. This control strategy would underlie not only intentional changes in the joint position, but also muscle relaxation. The notion that the motor cortex may control motor actions by shifting spatial frames of reference opens a new avenue in the analysis and understanding of brain function.

Figure 1. Threshold position control

The same shift in the threshold position of a body segment from R_i to R_f results in a change in the actual position of this segment in isotonic (zero load) condition (point a in A), in muscle torque in isometric condition (point b in B), or in both the position and muscle torque in intermediate condition (point c in C). Points a, b and c are equilibrium points defined as the points of intersection between the left continuous curve representing the final torque–angle characteristic (resulting from muscle activity regulated by proprioceptive feedback) and the dashed line (load torque–angle characteristic) in each panel.

Figure 2. Equalizing EMG activity at two wrist angles

A, subjects placed the hand in a vertical splint of a horizontal manipulandum and repeatedly flexed (F) and extended (E) the wrist. B and C, without compensation of the passive components of muscle forces, the tonic EMG activity of wrist flexors was higher when maintaining position F vs. E (F/E EMG ratio > 1). Similarly, extensors were more active at position E vs. F (E/F EMG ratio > 1, error bars are SDs). D–F, when passive wrist muscle forces were compensated by elastic, spring-like torques, the tonic EMG activity of each of 4 muscles substantially diminished and became position independent (EMG ratios ∼1.0). Asterisks indicate P < 0.001 for comparison of no-compensation with compensation ratios (Kolmogorov–Smirnov test). Representative data from one subject (S7).

Figure 3. Testing motoneuronal excitability at the actively established positions E and F based on early EMG SRs to perturbations

A, perturbations in the extension direction elicited a short-latency SR in wrist flexors (FCR, FCU) and a later response in extensors (ECR, ECU). B, perturbations in the flexion direction elicited a short-latency SR in stretched extensors and a later response in flexors. C, pre-perturbation EMG levels in position E and F (normalized to the maximal SR amplitude, individually for each muscle and subject) were similar (P > 0.05). D and E, earliest (30 ms duration) EMG SRs were also similar at the two positions.

Figure 4. Muscle relaxation

A, absence of EMG responses of fully relaxed wrist muscles to passive movements in the whole biomechanical joint range. B, in contrast to active wrist positioning (Fig. 3), no SR occurred in response to force pulses in relaxed muscles.

Figure 5. Muscle stiffness in threshold and relaxation states

Although EMG activity was minimal at both wrist positions (F and E), wrist stiffness (the slope of torque–angle characteristic) during active wrist position control was substantially higher than during full muscle relaxation at the same positions but established passively.

Figure 6. Typical mechanical and EMG responses to TMS at two static actively established positions, F and E, when the EMG activity and excitability of motoneurons of wrist muscles were equalized (as inFig. 3)

A, the left panel shows the wrist angle and MEPs for 4 wrist muscles at position E before movement. The next panel shows EMG activity during wrist movement from position E to position F at which a second TMS pulse was delivered. The last 2 panels show movement to position E and kinematic and EMG responses to TMS pulse at this position. The same TMS pulse elicited a flexor jerk at position F and an extensor jerk at position E (vertical arrows). Although the excitability of motoneurons was similar at the two positions, flexor MEPs at position F were substantially bigger than at position E and vice versa for extensor MEPs (reciprocal pattern). B, pre-TMS EMG levels in position E and F (normalized as in Fig. 3C) were similar (P > 0.05). C, group mean MEP amplitudes for 16 subjects.

Figure 7. Corticospinal excitability reflects the state of M1 that is specific to each wrist position, regardless of how it was reached

A, mean normalized MEP amplitudes at extension position (E = 20 deg) that was reached either by wrist flexion from position E +20 deg or by extension from position E –20 deg. B, similar test for a flexion position (F =−20 deg), after leaving a more extended or more flexed position. Error bars indicate SDs. Reaching direction had no effect on MEPs (P > 0.1; data for 6 subjects).

Figure 8. Responses to TMS (intensity as inFig. 6) at positions E and F established passively, by the experimenter, after muscle relaxation

A, compared to active specifications of wrist positions (Fig. 6A), mechanical responses to TMS (jerks) were absent and MEPs substantially diminished. B, pre-TMS EMG levels in position E and F (normalized as in Fig. 3C) were similar (P > 0.05). C, group mean normalized MEP amplitudes. After relaxation, position-related changes in MEP amplitudes were observed only for 2 of 4 muscles. D, histogram for the group showing a decrease in MEP amplitudes for all muscles after relaxation compared to those in active positioning, at both wrist positions.

Figure 9. Physiological origin of threshold position control and explanation of basic findings

A, integration of position-dependent proprioceptive (lower diagonal line) and position-independent central inputs (vertical arrow) to a flexor α-motoneuron. The central input shifts the threshold position for motoneuronal recruitment (R_e→R_f). B, full muscle relaxation in the whole biomechanical joint range [Q₋, Q₊] is achieved by minimizing the corticospinal facilitatory influences as well as those of other descending systems such that the threshold angle appears outside that range (R₊ > Q₊ for flexors, R₋ < Q₋ for extensors). Following the decrease in corticospinal facilitation and excitability of motoneurons, TMS responses in relaxed muscles are diminished compared to responses to TMS pulses applied during active wrist positioning.