The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction

Abstract

The motor cortex assumes an increasingly important role in higher mammals relative to that in lower mammals. This is true to such an extent that the human motor cortex is deeply involved in reflex regulation and it is common to speak of "transcortical reflex loops." Such loops appear to add flexibility to the human stretch reflex, once considered to be immutable, allowing it to adapt across a range of functional tasks. However, the purpose of this adaptation remains unclear. A common proposal is that stretch reflexes contribute to the regulation of limb stability; increased reflex sensitivity during tasks performed in unstable environments supports this hypothesis. Alternatively, before movement onset, stretch reflexes can assist an imposed stretch, opposite to what would be expected from a stabilizing response. Here we show that stretch reflex modulation in tasks that require changes in limb stability is mediated by motor cortical pathways, and that these differ from pathways contributing to reflex modulation that depend on how the subject is instructed to react to an imposed perturbation. By timing muscle stretches such that the modulated portion of the reflex occurred within a cortical silent period induced by transcranial magnetic stimulation, we abolished the increase in reflex sensitivity observed when individuals stabilized arm posture within a compliant environment. Conversely, reflex modulation caused by altered task instruction was unaffected by cortical silence. These results demonstrate that task-dependent changes in reflex function can be mediated through multiple neural pathways and that these pathways have task-specific roles.

Figure 1.

A, Participants were required to reach and hold a target level of endpoint force before a perturbation was triggered. Endpoint force was measured along the x-axis of the linear actuator. Visual feedback was provided as shown with a green column representing the instantaneous force level and a horizontal bar indicating the target force range (5 ± 1% elbow flexion MVC). B, Ramp-and-hold perturbations delivered by the linear actuator moved the wrist 30 mm along the −x-axis, thus extending the elbow joint and stretching the biceps brachii muscle. The actuator controller remained stiff throughout Stiff:DNI and Stiff:Resist trials and switched rapidly from compliant to stiff during Compliant:DNI trials to ensure consistent joint displacements. The duration of the perturbation was different in each experiment to alter the amplitude of the stretch response and avoid contamination of the reflex response by the end stop of the perturbation. C, Participants were seated comfortably facing a visual display at a distance of ∼1 m on which the force feedback was provided. Their arm was supported along the humerus by a cradle and at the wrist by a linear actuator. D, The three experiments in the current study examined the effect of changes in task instruction (“Do not intervene” and “Resist” the perturbation) and mechanical environment (Stiff and Compliant) on the amplitude of the long latency stretch response. Experiment 1 compares experimental conditions in which one of each of the task variables is altered from the baseline (Stiff:DNI) condition. Experiments 2 and 3 represent control experiments that serve to eliminate potential confounding variables.

Figure 2.

Cortical silence reduces the modulation of long-latency stretch responses due to changes in mechanical environment but not task instruction. A, Representative data from a single participant showing the response of the BB to stretches imposed at time 0 during low-level (5% MVC) activation. Mean data obtained from 20 consecutive trials are shown in this figure. Short-latency reflex (SLR) and long-latency reflex (LLR) components are evident at latencies of 23 ms and 62 ms respectively. B, A single trial is shown in which TMS was applied during a contraction of the biceps brachii at 5% MVC. The silent period following the excitatory motor evoked potential lasts longer than 150 ms following the TMS trigger. C, Data from the same participant as in A show reductions in the LLRs obtained within a period of cortical silence in the Stiff:DNI and Compliant:DNI conditions. No reduction in LLR amplitude is evident in the Stiff:Resist condition. D, Group means (±95% confidence intervals) are shown for background muscle activity (BGA), SLRs, and LLRs in each experimental condition. The 20 ms windows used to determine the amplitudes at each time point are shown in A and C. *Statistically significant difference (p < 0.05).

Figure 3.

Cortical silence reduces long-latency stretch responses in the Compliant:DNI but not Stiff:Resist condition. A, Representative data from a single participant demonstrates the equivalence of background levels of BB activity and the amplitude of the LLR to a series of imposed 100 ms muscle stretches. Mean responses from 20 trials in each condition are shown in this figure. B, During the period of TMS-induced cortical silence the LLR response is reduced during the Compliant:DNI condition but increased during the Stiff:Resist condition. C, Group means (±95% confidence intervals) demonstrate reductions in SLR amplitude following TMS. Statistically significant (*p < 0.05) differences between LLR amplitudes with and without TMS were also observed in both conditions.

Figure 4.

The amplitude of long-latency responses in the Stiff:Resist condition is independent of cortical silence. A, Representative data from a single participant demonstrates similar long-latency responses in the Stiff:Resist condition whether or not the elbow perturbation is preceded by TMS. B, Representative data from the same participant as in A demonstrate that long-latency responses in the Compliant:Resist condition also remain similar with and without TMS. C, Group mean data show that the amplitude of the long-latency response is not influenced by cortical inhibition. A reduction in the amplitude of the SLR is observable, however, indicating a pattern of TMS-induced inhibition similar to that observed in experiments 1 and 2.