Human Muscle Spindle Sensitivity Reflects the Balance of Activity between Antagonistic Muscles

Abstract

Muscle spindles are commonly considered as stretch receptors encoding movement, but the functional consequence of their efferent control has remained unclear. The "␣-␥ coactivation" hypothesis states that activity in a muscle is positively related to the output of its spindle afferents. However, in addition to the above, possible reciprocal inhibition of spindle controllers entails a negative relationship between contractile activity in one muscle and spindle afferent output from its antagonist. By recording spindle afferent responses from alert humans using microneurography, I show that spindle output does reflect antagonistic muscle balance. Specifically, regardless of identical kinematic profiles across active finger movements, stretch of the loaded antagonist muscle (i.e., extensor) was accompanied by increased afferent firing rates from this muscle compared with the baseline case of no constant external load. In contrast, spindle firing rates from the stretching antagonist were lowest when the agonist muscle powering movement (i.e., flexor) acted against an additional resistive load. Stepwise regressions confirmed that instantaneous velocity, extensor, and flexor muscle activity had a significant effect on spindle afferent responses, with flexor activity having a negative effect. Therefore, the results indicate that, as consequence of their efferent control, spindle sensitivity (gain) to muscle stretch reflects the balance of activity between antagonistic muscles rather than only the activity of the spindle-bearing muscle.

Neuromorphic meets neuromechanics, part II: the role of fusimotor drive

“…Therefore, we added a scaling factor in the form of an offset and gain to increase firing rates to a level that was able to appropriately drive their respective motor neuron pools. This is why the firing rates for the spindle afferents in Figure 6 are higher than those seen in spindle afferents which rarely fire faster than 250pps [17,36]. However, we believe that this does not affect the validity of our results, and will not be necessary once we are able to implement thousands of spindle afferents.…”

Quantifying Nonlinear Contributions to Cortical Responses Evoked by Continuous Wrist Manipulation

“…In the active task the muscles are generating force due to both co-contraction and reflexive activity, resulting in increased wrist torque. Compared to the passive task, this will result in changed muscle spindle sensitivity [37] and an increase in output of the Golgi tendon organ [38]. Changes in EEG could also be due to the involvement of additional brain regions in voluntary cocontraction during the active task (e.g., supplementary motor area, pre-motor cortex, posterior parietal cortex) [39].…”

Muscle Spindles and Locomotor Control-An Unrecognized Falls Determinant?

“…In addition to the aforementioned studies, some research has been forthcoming to examine if muscle spindles can mediate both intra as well as interlimb coordination processes that are needed during gait. In this regard, although Dimitrou [28] did not study locomotion, this group found muscle spindles are able to modulate the desired outputs to the moving as well as the stationary limb due to their ability to convey ongoing information on position, both initial, subsequent and final, while remaining sensitive to efferent inputs and prevailing activity of the antagonistic muscles. That is, once one movement in the gait cycle has occurred, the muscle afferents can respond by helping to initiate a subsequent movement that is consistent with the magnitude of force needed to ensure stability, safety and efficiency.…”

“…Research also shows that in addition to its role in stability control during locomotion, the negative relationship between the contractile activity in one muscle and the spindle afferent output from its antagonist during walking movements is of high import in enabling the organism to carry out these reciprocal movements, in a timely way [28] . Indeed, whereas, some of this regulatory information may come from other sources, or may be of minor import in day to day non-varying walking situations, the presence of stretch sensitive nerve endings in the key muscles of locomotion appears to provide the central nervous system with an up dated set of inputs during on-going activities [29] that may not only be crucial for producing optimal stability, but also for exhibiting resistance to obstacles placed in the walkers path [27] .…”