Threshold position control of anticipation in humans: a possible role of corticospinal influences

Abstract

Key points: Sudden unloading of preloaded wrist muscles elicits motion to a new wrist position. Such motion is prevented if subjects unload muscles using the contralateral arm (self-unloading). Corticospinal influences originated from the primary motor cortex maintain tonic influences on motoneurons of wrist muscles before sudden unloading but modify these influences prior to the onset and until the end of self-unloading. Results are interpreted based on the previous finding that intentional actions are caused by central, particularly corticospinal, shifts in the spatial thresholds at which wrist motoneurons are activated, thus predetermining the attractor point at which the neuromuscular periphery achieves mechanical balance with environment forces. By maintaining or shifting the thresholds, descending systems let body segments go to the equilibrium position in the respective unloading tasks without the pre-programming of kinematics or muscle activation patterns. The study advances the understanding of how motor actions in general, and anticipation in particular, are controlled.

Abstract: The role of corticospinal (CS) pathways in anticipatory motor actions was evaluated using transcranial magnetic stimulation (TMS) of the primary motor cortex projecting to motoneurons (MNs) of wrist muscles. Preloaded wrist flexors were suddenly unloaded by the experimenter or by the subject using the other hand (self-unloading). After sudden unloading, the wrist joint involuntarily flexed to a new position. In contrast, during self-unloading the wrist remained almost motionless, implying that an anticipatory postural adjustment occurred. In the self-unloading task, anticipation was manifested by a decrease in descending facilitation of pre-activated flexor MNs starting ∼72 ms before changes in the background EMG activity. Descending facilitation of extensor MNs began to increase ∼61 ms later. Conversely, these influences remained unchanged before sudden unloading, implying the absence of anticipation. We also tested TMS responses during EMG silent periods produced by brief muscle shortening, transiently resulting in similar EMG levels before the onset and after the end of self-unloading. We found reduced descending facilitation of flexor MNs after self-unloading. To explain why the wrist excursion was minimized in self-unloading due to these changes in descending influences, we relied on previous demonstrations that descending systems pre-set the threshold positions of body segments at which muscles begin to be activated, thus predetermining the equilibrium point to which the system is attracted. Based on this notion, a more consistent explanation of the kinematic, EMG and descending patterns in the two types of unloading is proposed compared to the alternative notion of direct pre-programming of kinematic and/or EMG patterns.

Keywords: behavioural neuroscience; control variables; motor cortex.

Figure 1. Threshold position control of muscle activation and force

A, muscle is active when the difference between the actual muscle length x and the dynamic threshold muscle length λ^* for recruitment of the smallest motor unit is positive; λ^* depends on central influences on λ, sensitivity μ to stretch velocity v and on parameter ρ comprising effects of intermuscular interaction, cutaneous influences and effects of plateau potentials. The number (n) of recruited motor units increases with the increasing difference between the actual muscle length and the dynamic threshold length. B, active muscle force also increases with this difference. C, the physiological origin of the muscle activation threshold and its central regulation. The membrane potential of an initially inactive MN increases with muscle stretching (lower diagonal line), and when the potential reaches the electrical threshold at some threshold muscle length (λ) the MN is activated. This spatial threshold decreases by Δλ if the membrane potential is enhanced (ΔV) via independent central inputs to the MN (upper diagonal line). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2. Typical kinematics and EMG patterns during sudden unloading and self‐unloading of the wrist

A, initially, external torque transmitted to the palm of the wrist via a plastic board (grey rectangle) was compensated by wrist flexors. When the load was suddenly removed (sudden unloading), the wrist involuntary flexed to a final position. B, when the subject removed the load using the other hand (self‐unloading), the wrist remained almost motionless. C and D, wrist angle and EMG patterns of flexor (FCR, FCU) and extensor (ECR and ECU) muscles during two unloading tasks in a representative subject (S6). Self‐unloading onset (right vertical line in D is the time when flexor EMG levels began to decrease. E and F, mean ± SD EMG levels of wrist muscles at the initial and final positions for the group of 10 subjects. With transition to the final position, flexor EMG levels decreased in both unloading tasks but extensor EMG levels increased only in the self‐unloading task (F). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3. Examples of mechanical and EMG responses to TMS before self‐unloading onset

A, mechanical responses of wrist muscles decreased before self‐unloading onset (subject S10). Responses to TMS were triggered in 15 trials about 2.2 s (upper curves, mean ± SD) or 75 ms before the self‐unloading onset; traces were aligned according to the time of the TMS trigger. B and C, Pattern 1: flexor MEPs (mean ± SD) decreased while extensor MEPs did not change before the self‐unloading (subject S4); Pattern 2: flexor MEPs did not change but extensor MEPs increased (subject S9). MEPs were obtained in response to TMS 2 s before (left panel) or 170 ms after go signal (right panel). Right panels in A–C show similarities in EMG levels before the self‐unloading onset, as confirmed by an equivalence test (see Results); EMG levels 2 s before (left bars) are compared with those 0.12 s (in A) and 0.17 s (B and C) after go signal. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4. Corticospinal influences before the self‐unloading onset

A, in 6 subjects (left panel), flexor MEPs decreased without changes in extensor MEPs while in another 4 subjects (middle and right columns) extensor MEPs increased, in the absence of changes in flexor MEPs (in S9) or in combination with a decrease in MEPs of one flexor (S10) or both flexors (S2, S7). Each dot represents the normalized MEPs (averaged from 15 trials) at different times before the self‐unloading onset (time 0). B, EMG levels before each point of MEP measurement in A were similar (equivalence test) for the group (see Results).

Figure 5. Transiently equalizing EMG levels by brief muscle shortening before and after self‐unloading in the TMS conditioning technique

A, silent EMG periods in shortening flexors and EMG bursts in stretched extensors (subject S14). B, EMG levels of flexor muscles before and after self‐unloading (mean ± SD), for the group of 9 subjects. The first bar for each muscle shows the tonic EMG level at the initial position in the absence of muscle shortening. C, similarity in the EMG levels during silent periods elicited before and during a steady state after self‐unloading, as confirmed by an equivalence test (see Results). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 6. Cortical influences before and after self‐unloading onset, evaluated by the TMS conditioning technique (MEPs were produced during EMG silent periods elicited by muscle shortening to transiently equalize EMG levels, as shown in Fig. 5)

A, upper trace shows wrist angle during self‐unloading task in subject S11. Lower traces are MEPs (mean ± SD) obtained 2 s before and 5 s after the go signal to self‐unloading. Both flexor MEPs decreased after self‐unloading onset. B, group results for 9 subjects (S2, S5, S8, S11–S16), showing that corticospinal influences on flexors decreased after self‐unloading (^* P < 0.02). MEP amplitudes were normalized by the maximal MEP values before the unloading onset, individually for each muscle and subject. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 7. By initiating shifts in the threshold position at which MNs begin to be recruited prior to changes in the muscle activity, descending systems can minimize the wrist motion in the self‐unloading task (schematic diagrams)

A, in order to establish the required initial wrist position while compensating a load (dashed horizontal line) that tends to extend the wrist joint, descending systems specify appropriate threshold joint angles (R _F and R _E). Resulting flexor activity and torque balance the load at the initial position. Following sudden unloading, the equilibrium point of the system is mechanically shifted from point a to point b located within a small coactivation zone (between R _F and R _E). Muscle‐reflex properties are sufficient to accomplish movement to point b while the influences of descending systems may remain unchanged. B, in contrast, in anticipation of self‐unloading, descending systems can start decreasing facilitation of flexor MNs and increasing facilitation of extensor MNs before the unloading onset, thus shifting the spatial flexor and extensor thresholds and torque‐angle characteristics in the same direction, towards the initial position. This process can also increase the coactivation zone. As a result, the system prevents motion to point b by setting equilibrium point c, thus minimizing the wrist deflection from the initial position. [Color figure can be viewed at wileyonlinelibrary.com]