Fast corrective responses are evoked by perturbations approaching the natural variability of posture and movement tasks

2012 ◽  
Vol 107 (10) ◽  
pp. 2821-2832 ◽  
Author(s):  
F. Crevecoeur ◽  
I. Kurtzer ◽  
S. H. Scott

A wealth of studies highlight the importance of rapid corrective responses during voluntary motor tasks. These studies used relatively large perturbations to evoke robust muscle activity. Thus it remains unknown whether these corrective responses (latency 20–100 ms) are evoked at perturbation levels approaching the inherent variability of voluntary control. To fill this gap, we examined responses for large to small perturbations applied while participants either performed postural or reaching tasks. To address multijoint corrective responses, we induced various amounts of single-joint elbow motion with scaled amounts of combined elbow and shoulder torques. Indeed, such perturbations are known to elicit a response at the unstretched shoulder muscle, which reflects an internal model of arm intersegmental dynamics. Significant muscle responses were observed during both postural control and reaching, even when perturbation-related joint angle, velocity, and acceleration overlapped in distribution with deviations encountered in unperturbed trials. The response onsets were consistent across the explored range of perturbation loads, with short-latency onset for the muscles spanning the elbow joints (20–40 ms), and long-latency for shoulder muscles (onset > 45 ms). In addition, the evoked activity was strongly modulated by perturbation magnitude. These results suggest that multijoint responses are not specifically engaged to counter motor errors that exceed a certain threshold. Instead, we suggest that these corrective processes operate continuously during voluntary motor control.

2016 ◽  
Vol 116 (5) ◽  
pp. 2236-2249 ◽  
Author(s):  
Jeffrey Weiler ◽  
James Saravanamuttu ◽  
Paul L. Gribble ◽  
J. Andrew Pruszynski

The long-latency stretch response (muscle activity 50–100 ms after a mechanical perturbation) can be coordinated across multiple joints to support goal-directed actions. Here we assessed the flexibility of such coordination and whether it serves to counteract intersegmental dynamics and exploit kinematic redundancy. In three experiments, participants made planar reaches to visual targets after elbow perturbations and we assessed the coordination of long-latency stretch responses across shoulder, elbow, and wrist muscles. Importantly, targets were placed such that elbow and wrist (but not shoulder) rotations could help transport the hand to the target—a simple form of kinematic redundancy. In experiment 1 we applied perturbations of different magnitudes to the elbow and found that long-latency stretch responses in shoulder, elbow, and wrist muscles scaled with perturbation magnitude. In experiment 2 we examined the trial-by-trial relationship between long-latency stretch responses at adjacent joints and found that the magnitudes of the responses in shoulder and elbow muscles, as well as elbow and wrist muscles, were positively correlated. In experiment 3 we explicitly instructed participants how to use their wrist to move their hand to the target after the perturbation. We found that long-latency stretch responses in wrist muscles were not sensitive to our instructions, despite the fact that participants incorporated these instructions into their voluntary behavior. Taken together, our results indicate that, during reaching, the coordination of long-latency stretch responses across multiple joints counteracts intersegmental dynamics but may not be able to exploit kinematic redundancy.


2015 ◽  
Vol 114 (6) ◽  
pp. 3242-3254 ◽  
Author(s):  
Jeffrey Weiler ◽  
Paul L. Gribble ◽  
J. Andrew Pruszynski

Many studies have demonstrated that muscle activity 50–100 ms after a mechanical perturbation (i.e., the long-latency stretch response) can be modulated in a manner that reflects voluntary motor control. These previous studies typically assessed modulation of the long-latency stretch response from individual muscles rather than how this response is concurrently modulated across multiple muscles. Here we investigated such concurrent modulation by having participants execute goal-directed reaches to visual targets after mechanical perturbations of the shoulder, elbow, or wrist while measuring activity from six muscles that articulate these joints. We found that shoulder, elbow, and wrist muscles displayed goal-dependent modulation of the long-latency stretch response, that the relative magnitude of participants' goal-dependent activity was similar across muscles, that the temporal onset of goal-dependent muscle activity was not reliably different across the three joints, and that shoulder muscles displayed goal-dependent activity appropriate for counteracting intersegmental dynamics. We also observed that the long-latency stretch response of wrist muscles displayed goal-dependent modulation after elbow perturbations and that the long-latency stretch response of elbow muscles displayed goal-dependent modulation after wrist perturbations. This pattern likely arises because motion at either joint could bring the hand to the visual target and suggests that the nervous system rapidly exploits such simple kinematic redundancy when processing sensory feedback to support goal-directed actions.


2015 ◽  
Vol 113 (1) ◽  
pp. 192-202 ◽  
Author(s):  
Joseph Y. Nashed ◽  
Isaac L. Kurtzer ◽  
Stephen H. Scott

A number of studies have highlighted the sophistication of corrective responses in lengthened muscles during the long-latency epoch. However, in various contexts, unloading can occur, which requires corrective actions from a shortened muscle. Here, we investigate the sophistication of inhibitory responses in shortened muscles due to unloading. Our first experiment quantified the inhibitory responses following an unloading torque that displaced the hand either into or away from a peripheral target. We observed larger long-latency inhibitory responses when perturbed into the peripheral target compared with away from the target. In our second experiment, we characterized the degree of inhibition following unloading with respect to different levels of preperturbation muscle activity. We initially observed that the inhibitory activity during the short-latency epoch scaled with increased levels of preperturbation muscle activity. However, this scaling peaked early in the R2 epoch (∼50 ms) but then quickly diminished through the rest of the long-latency epoch. Finally, in experiment 3, we investigated whether inhibitory perturbation responses consider intersegmental dynamics of the limb. We quantified unloading responses for either pure shoulder or pure elbow torques that evoked similar motion at the shoulder but different elbow motion. The long-latency inhibitory response in the shoulder, unlike the short-latency, was greater for the shoulder torque compared with the response following an elbow torque, as previously observed for a loading response. Taken together, these results illustrate that the long-latency unloading response is capable of a similar level of complexity as observed when loads are applied to the limb.


2016 ◽  
Vol 115 (4) ◽  
pp. 2176-2190 ◽  
Author(s):  
Isaac Kurtzer ◽  
Jenna Meriggi ◽  
Nidhi Parikh ◽  
Kenneth Saad

Postural corrections of the upper limb are required in tasks ranging from handling an umbrella in the changing wind to securing a wriggling baby. One complication in this process is the mechanical interaction between the different segments of the arm where torque applied at one joint induces motion at multiple joints. Previous studies have shown the long-latency reflexes of shoulder muscles (50–100 ms after a limb perturbation) account for these mechanical interactions by integrating information about motion of both the shoulder and elbow. It is less clear whether long-latency reflexes of elbow muscles exhibit a similar capability and what is the relation between the responses of shoulder and elbow muscles. The present study utilized joint-based loads tailored to the subjects' arm dynamics to induce well-controlled displacements of their shoulder and elbow. Our results demonstrate that the long-latency reflexes of shoulder and elbow muscles integrate motion from both joints: the shoulder and elbow flexors respond to extension at both joints, whereas the shoulder and elbow extensors respond to flexion at both joints. This general pattern accounts for the inherent flexion-extension coupling of the two joints arising from the arm's intersegmental dynamics and is consistent with spindle-based reciprocal excitation of shoulder and elbow flexors, reciprocal excitation of shoulder and elbow extensors, and across-joint inhibition between the flexors and extensors.


2013 ◽  
Vol 109 (8) ◽  
pp. 2228-2241 ◽  
Author(s):  
Isaac Kurtzer ◽  
Paxson Trautman ◽  
Russell J. Rasquinha ◽  
Nasir H. Bhanpuri ◽  
Stephen H. Scott ◽  
...  

Damage to the cerebellum can cause significant problems in the coordination of voluntary arm movements. One prominent idea is that incoordination stems from an inability to predictively account for the complex mechanical interactions between the arm's several joints. Motivated by growing evidence that corrective feedback control shares important capabilities and neural substrates with feedforward control, we asked whether cerebellar damage impacts feedback stabilization of the multijoint arm appropriate for the arm's intersegmental dynamics. Specifically, we tested whether cerebellar dysfunction impacts the ability of posterior deltoid to incorporate elbow motion in its long-latency response (R2 = 45–75 ms and R3 = 75–100 ms after perturbation) to an unexpected torque perturbation. Healthy and cerebellar-damaged subjects were exposed to a selected pattern of shoulder-elbow displacements to probe the response pattern from this shoulder extensor muscle. The healthy elderly subjects expressed a long-latency response linked to both shoulder and elbow motion, including an increase/decrease in shoulder extensor activity with elbow flexion/extension. Critically, cerebellar-damaged subjects displayed the normal pattern of activity in the R3 period indicating an intact ability to rapidly integrate multijoint motion appropriate to the arm's intersegmental dynamics. However, cerebellar-damaged subjects had a lower magnitude of activity that was specific to the long-latency period (both R2 and R3) and a slightly delayed onset of multijoint sensitivity. Taken together, our results suggest that the basic motor pattern of the long-latency response is housed outside the cerebellum and is scaled by processes within the cerebellum.


1999 ◽  
Vol 82 (5) ◽  
pp. 2310-2326 ◽  
Author(s):  
Paul L. Gribble ◽  
David J. Ostry

During multijoint limb movements such as reaching, rotational forces arise at one joint due to the motions of limb segments about other joints. We report the results of three experiments in which we assessed the extent to which control signals to muscles are adjusted to counteract these “interaction torques.” Human subjects performed single- and multijoint pointing movements involving shoulder and elbow motion, and movement parameters related to the magnitude and direction of interaction torques were manipulated systematically. We examined electromyographic (EMG) activity of shoulder and elbow muscles and, specifically, the relationship between EMG activity and joint interaction torque. A first set of experiments examined single-joint movements. During both single-joint elbow ( experiment 1) and shoulder ( experiment 2) movements, phasic EMG activity was observed in muscles spanning the stationary joint (shoulder muscles in experiment 1 and elbow muscles in experiment 2). This muscle activity preceded movement and varied in amplitude with the magnitude of upcoming interaction torque (the load resulting from motion of the nonstationary limb segment). In a third experiment, subjects performed multijoint movements involving simultaneous motion at the shoulder and elbow. Movement amplitude and velocity at one joint were held constant, while the direction of movement about the other joint was varied. When the direction of elbow motion was varied (flexion vs. extension) and shoulder kinematics were held constant, EMG activity in shoulder muscles varied depending on the direction of elbow motion (and hence the sign of the interaction torque arising at the shoulder). Similarly, EMG activity in elbow muscles varied depending on the direction of shoulder motion for movements in which elbow kinematics were held constant. The results from all three experiments support the idea that central control signals to muscles are adjusted, in a predictive manner, to compensate for interaction torques—loads arising at one joint that depend on motion about other joints.


2020 ◽  
Vol 2020 ◽  
pp. 1-13
Author(s):  
Elodie Traverse ◽  
Clémentine Brun ◽  
Émilie Harnois ◽  
Catherine Mercier

Movement is altered by pain, but the underlying mechanisms remain unclear. Assessing corrective muscle responses following mechanical perturbations can help clarify these underlying mechanisms, as these responses involve spinal (short-latency response, 20-50 ms), transcortical (long-latency response, 50-100 ms), and cortical (early voluntary response, 100-150 ms) mechanisms. Pairing mechanical (proprioceptive) perturbations with different conditions of visual feedback can also offer insight into how pain impacts on sensorimotor integration. The general aim of this study was to examine the impact of experimental tonic pain on corrective muscle responses evoked by mechanical and/or visual perturbations in healthy adults. Two sessions (Pain (induced with capsaicin) and No pain) were performed using a robotic exoskeleton combined with a 2D virtual environment. Participants were instructed to maintain their index in a target despite the application of perturbations under four conditions of sensory feedback: (1) proprioceptive only, (2) visuoproprioceptive congruent, (3) visuoproprioceptive incongruent, and (4) visual only. Perturbations were induced in either flexion or extension, with an amplitude of 2 or 3 Nm. Surface electromyography was recorded from Biceps and Triceps muscles. Results demonstrated no significant effect of the type of sensory feedback on corrective muscle responses, no matter whether pain was present or not. When looking at the effect of pain on corrective responses across muscles, a significant interaction was found, but for the early voluntary responses only. These results suggest that the effect of cutaneous tonic pain on motor control arises mainly at the cortical (rather than spinal) level and that proprioception dominates vision for responses to perturbations, even in the presence of pain. The observation of a muscle-specific modulation using a cutaneous pain model highlights the fact that the impacts of pain on the motor system are not only driven by the need to unload structures from which the nociceptive signal is arising.


1989 ◽  
Vol 257 (2) ◽  
pp. R410-R421 ◽  
Author(s):  
B. Mallory ◽  
W. D. Steers ◽  
W. C. De Groat

Electrophysiological techniques were used to examine the asynchronous and evoked activity on postganglionic nerves to the urinary bladder in the urethananesthetized rat. Distension of the bladder (0.4-0.6 ml) evoked reflex contractions of the bladder (mean intravesical pressure 28 cmH2O) and efferent firing on postganglionic nerves. Electrical stimulation of afferent and efferent axons in the pelvic nerve elicited short-latency (0.3-11 ms) responses and long-latency (45-170 ms) reflexes on the nerves. The short-latency responses consisted of nonsynaptic axonal volleys with conduction velocities ranging from 0.5 to 11 m/s and synaptic responses with latencies of 6-11 ms. Stimulation of the pelvic nerve elicited late supraspinal reflexes (mean latency 122 +/- 28 ms) in 60% of normal rats and an early reflex (mean latency 56 +/- 5 ms) in 25% of those animals in which a late reflex was also identified. Early reflexes (mean latency 50 +/- 9 ms) were elicited in 100% of chronic spinal animals. The conduction time for the afferent and efferent limbs of the reflexes was calculated to be 7 and 58 ms, respectively, with a central delay of 57 ms for the late and less than 5 ms for the early reflex. It is concluded that sacral parasympathetic input to the urinary bladder of the rat is mediated by supraspinal and spinal reflex pathways. It is likely that in normal animals the late-occurring supraspinal reflex mediates micturition. The significance of the spinal reflex in the normal animals is uncertain; however, this reflex is essential for the generation of automatic micturition in chronic spinal preparations.


2020 ◽  
Author(s):  
Rodrigo S. Maeda ◽  
Rhonda Kersten ◽  
J. Andrew Pruszynski

AbstractPrevious work has shown that humans account for and learn novel properties or the arm’s dynamics, and that such learning causes changes in both the predictive (i.e., feedforward) control of reaching and reflex (i.e., feedback) responses to mechanical perturbations. Here we show that similar observations hold in old-world monkeys (macaca fascicularis). Two monkeys were trained to use an exoskeleton to perform a single-joint elbow reaching and to respond to mechanical perturbations that created pure elbow motion. Both of these tasks engaged robust shoulder muscle activity as required to account for the torques that typically arise at the shoulder when the forearm rotates around the elbow joint (i.e., intersegmental dynamics). We altered these intersegmental arm dynamics by having the monkeys generate the same elbow movements with the shoulder joint either free to rotate, as normal, or fixed by the robotic manipulandum, which eliminates the shoulder torques caused by forearm rotation. After fixing the shoulder joint, we found a systematic reduction in shoulder muscle activity. In addition, after releasing the shoulder joint again, we found evidence of kinematic aftereffects (i.e., reach errors) in the direction predicted if failing to compensate for normal arm dynamics. We also tested whether such learning transfers to feedback responses evoked by mechanical perturbations and found a reduction in shoulder feedback responses, as appropriate for these altered arm intersegmental dynamics. Demonstrating this learning and transfer in non-human primates will allow the investigation of the neural mechanisms involved in feedforward and feedback control of the arm’s dynamics.


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