Michael Dimitriou

Task-dependent coordination of rapid bimanual motor responses

Optimal feedback control postulates that feedback responses depend on the task relevance of any perturbations. We test this prediction in a bimanual task, conceptually similar to balancing a laden tray, in which each hand could be perturbed up or down. Single-limb mechanical perturbations produced long-latency reflex responses (“rapid motor responses”) in the contralateral limb of appropriate direction and magnitude to maintain the tray horizontal. During bimanual perturbations, rapid motor responses modulated appropriately depending on the extent to which perturbations affected tray orientation. Specifically, despite receiving the same mechanical perturbation causing muscle stretch, the strongest responses were produced when the contralateral arm was perturbed in the opposite direction (large tray tilt) rather than in the same direction or not perturbed at all. Rapid responses from shortening extensors depended on a nonlinear summation of the sensory information from the arms, with the response to a bimanual same-direction perturbation (orientation maintained) being less than the sum of the component unimanual perturbations (task relevant). We conclude that task-dependent tuning of reflexes can be modulated online within a single trial based on a complex interaction across the arms.

The Temporal Evolution of Feedback Gains Rapidly Update to Task Demands

Recent theoretical frameworks such as optimal feedback control suggest that feedback gains should modulate throughout a movement and be tuned to task demands. Here we measured the visuomotor feedback gain throughout the course of movements made to “near” or “far” targets in human subjects. The visuomotor gain showed a systematic modulation over the time course of the reach, with the gain peaking at the middle of the movement and dropping rapidly as the target is approached. This modulation depends primarily on the proportion of the movement remaining, rather than hand position, suggesting that the modulation is sensitive to task demands. Model-predictive control suggests that the gains should be continuously recomputed throughout a movement. To test this, we investigated whether feedback gains update when the task goal is altered during a movement, that is when the target of the reach jumped. We measured the visuomotor gain either simultaneously with the jump or 100 ms after the jump. The visuomotor gain nonspecifically reduced for all target jumps when measured synchronously with the jump. However, the visuomotor gain 100 ms later showed an appropriate modulation for the revised task goal by increasing for jumps that increased the distance to the target and reducing for jumps that decreased the distance. We conclude that visuomotor feedback gain shows a temporal evolution related to task demands and that this evolution can be flexibly recomputed within 100 ms to accommodate online modifications to task goals.

Discharges in Human Muscle Receptor Afferents during Block Grasping

Human grasping relies on feedforward control that is monitored and corrected on-line by means of sensory feedback. While much of the sensory mechanisms underpinning hand-object interaction are known, information has been lacking about muscle receptor responses during the phases before and after actual object contact. We therefore let subjects use their thumb and fingers to grasp blocks presented to them while we recorded muscle afferents from the thumb and finger extensor muscles along with wrist and digit kinematics, and electromyographic activity. The kinematics of the task was indistinguishable from “normal” grasping. None of the afferents encoded either object contact or finger apposition. Both primary and secondary afferents were more phase advanced on the parent muscle lengths than expected from previous studies as well as from their responses to imposed length changes of their parent muscles. Thus, the discharges of both primary and secondary afferents were well correlated to the tendon velocity of their parent muscles and that of primary afferents also to acceleration whereas neither appeared to encode muscle length as such. Decoding the velocity of muscle length changes were significantly improved if the discharge of Golgi tendon organ afferents were taken into account along with that of the muscle spindle afferents. We propose that these findings may be explained by the biomechanical properties of contracting muscles. Moreover, we conclude that it seems unlikely that the muscle spindle afferents recorded in this task have any role in providing “proprioceptive” information pertaining to the size of an object grasped.

Discharges in human muscle spindle afferents during a key-pressing task

Most manual tasks demand a delicate control of the wrist. Sensory information for this control, e.g. about the position and movement velocity of the hand, is assumed to be primarily provided by muscle spindle afferents. It is known that human muscle spindles in relaxed muscles behave as stretch receptors but it is unclear how they discharge during ‘natural’ hand movements, since their discharges can also be affected by extrafusal contractions and fusimotor activity. We therefore let subjects perform a centre‐out‐centre key‐pressing task on buttons laid out in a 3 × 3 pattern, a task that allowed unconstrained hand and finger movements and required precise control of the wrist. Microneurography recordings from muscle spindle afferents of the wrist extensor muscles were obtained along with wrist kinematics and electromyographic signals. The discharge rates of afferents were more phase advanced than expected on the length of the radial wrist extensor, which acted as an anti‐gravity muscle in the key‐pressing task. As such, both acceleration and velocity had significant impacts on the discharge rate of primary afferents, velocity on that of secondary afferents, and length had no impact on either afferent type. The response patterns were different for the two types of muscle spindle afferents from the predominantly eccentrically contracting ulnar wrist extensor: muscle length and velocity had significant impacts on the ensemble response of secondary afferents whereas the primary afferents showed highly variable responses. Accordingly, good predictions of the radial ulnar angular velocity were possible from spindle ensemble responses (R2= 0.85) whereas length could be predicted only for phases with lengthening of the ulnar wrist extensor. There are several possible explanations for the unexpectedly large phase advance of spindle afferents in the radial wrist extensor. Given the compliance of tendons, for instance, the phase relationship between the muscle fascicle length and the whole muscle length is conjectured to depend on the load. While additional phase advances are advantageous in motor control, it is concluded that if the central nervous system estimates length or velocity of a muscle from its muscle spindle discharges, this would require additional information about not only the concomitant extrafusal and fusimotor drive but also about the mechanical properties of the load on which the muscle acts.

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

Muscle spindles are commonly considered as stretch receptors encoding movement, but the functional consequence of their efferent control has remained unclear. The “α–γ 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.

Task-dependent modulation of spinal and transcortical stretch reflexes linked to motor learning rate.

It is generally believed that task-dependent control of body configuration (“posture”) is achieved by adjusting voluntary motor activity and transcortical “long-latency” reflexes. Spinal monosynaptic circuits are thought not to be engaged in such task-level control. Similarly, being in a state of motor learning has been strongly associated only with an upregulation of feedback responses at transcortical latencies and beyond. In two separate experiments, the current study examined the task-dependent modulation of stretch reflexes by perturbing the hand of human subjects while they were waiting for a “Go” signal to move at the different stages of a classic kinematic learning task (visuomotor rotation). Although the subjects had to resist all haptic perturbations equally across task stages, the study leveraged that task-dependent feedback controllers may already be “loaded” at the movement anticipation stage. In addition to an upregulation of reflex gains during early exposure to the visual distortion, I found a relative inhibition of reflex responses in the “washout” stage (sensory realignment state). For more distal muscles (brachioradialis) this inhibition also extended to the monosynaptic reflex response (“R1”). Moreover, these R1 gains reflected individual motor learning performance in the visuomotor task. The results demonstrate that the system’s “control policy” in visuomotor adaptation can also include inhibition of proprioceptive reflexes, and that aspects of this policy can affect monosynaptic spinal circuits. The latter finding suggests a novel form of state-related control, probably realized by independent control of fusimotor neurons, through which segmental circuits can tune to higher-level features of a sensorimotor task.