Context-dependent inhibition of unloaded muscles during the long-latency epoch

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.

2009 ◽  
Vol 102 (2) ◽  
pp. 992-1003 ◽  
Author(s):  
J. Andrew Pruszynski ◽  
Isaac Kurtzer ◽  
Timothy P. Lillicrap ◽  
Stephen H. Scott

The earliest neural response to a mechanical perturbation, the short-latency stretch response (R1: 20–45 ms), is known to exhibit “automatic gain-scaling” whereby its magnitude is proportional to preperturbation muscle activity. Because gain-scaling likely reflects an intrinsic property of the motoneuron pool (via the size-recruitment principle), counteracting this property poses a fundamental challenge for the nervous system, which must ultimately counter the absolute change in load regardless of the initial muscle activity (i.e., show no gain-scaling). Here we explore the temporal evolution of gain-scaling in a simple behavioral task where subjects stabilize their arm against different background loads and randomly occurring torque perturbations. We quantified gain-scaling in four elbow muscles (brachioradialis, biceps long, triceps lateral, triceps long) over the entire sequence of muscle activity following perturbation onset—the short-latency response, long-latency response (R2: 50–75 ms; R3: 75–105 ms), early voluntary corrections (120–180 ms), and steady-state activity (750–1250 ms). In agreement with previous observations, we found that the short-latency response demonstrated substantial gain-scaling with a threefold increase in background load resulting in an approximately twofold increase in muscle activity for the same perturbation. Following the short-latency response, we found a rapid decrease in gain-scaling starting in the long-latency epoch (∼75-ms postperturbation) such that no significant gain-scaling was observed for the early voluntary corrections or steady-state activity. The rapid decrease in gain-scaling supports our recent suggestion that long-latency responses and voluntary control are inherently linked as part of an evolving sensorimotor control process through similar neural circuitry.


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.


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.


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.


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.


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.


2000 ◽  
Vol 84 (2) ◽  
pp. 1088-1092 ◽  
Author(s):  
Kemal S. Türker ◽  
Melissa Jenkins

The reflex response of the masseter muscle to the rapid unloading of a single maxillary incisor tooth was studied. Unloading of a static force of 2 N in the horizontal direction resulted in a short-latency excitation, inhibition, and long-latency excitation of masseter muscle activity occurring at latencies of approximately 13, 20, and 40 ms, respectively, with a corresponding change in bite force occurring slightly later in each case. Following the blocking of periodontal input by the injection of local anesthetic around the stimulated tooth, inhibitory responses were abolished. Therefore, it is concluded that the observed masseteric inhibition was caused by the unloading of periodontal mechanoreceptors and thus that these receptors may contribute to the jaw unloading reflex.


2012 ◽  
Vol 108 (4) ◽  
pp. 999-1009 ◽  
Author(s):  
Joseph Y. Nashed ◽  
Frédéric Crevecoeur ◽  
Stephen H. Scott

The motor system must consider a variety of environmental factors when executing voluntary motor actions, such as the shape of the goal or the possible presence of intervening obstacles. It remains unknown whether rapid feedback responses to mechanical perturbations also consider these factors. Our first experiment quantified how feedback corrections were altered by target shape, which was either a circular dot or a bar. Unperturbed movements to each target were qualitatively similar on average but with greater dispersion of end point positions when reaching to the bar. On random trials, multijoint torque perturbations deviated the hand left or right. When reaching to a circular target, perturbations elicited corrective movements that were directed straight to the location of the target. In contrast, corrective movements when reaching to a bar were redirected to other locations along the bar axis. Our second experiment quantified whether the presence of obstacles could interfere with feedback corrections. We found that hand trajectories after the perturbations were altered to avoid obstacles in the environment. Importantly, changes in muscle activity reflecting the different target shapes (bar vs. dot) or the presence of obstacles were observed in as little as 70 ms. Such changes in motor responses were qualitatively consistent with simulations based on optimal feedback control. Taken together, these results highlight that long-latency motor responses consider spatial properties of the goal and environment.


1989 ◽  
Vol 62 (3) ◽  
pp. 711-722 ◽  
Author(s):  
T. Allison ◽  
G. McCarthy ◽  
C. C. Wood ◽  
P. D. Williamson ◽  
D. D. Spencer

1. The anatomic generators of human median nerve somatosensory evoked potentials (SEPs) in the 40 to 250-ms latency range were investigated in 54 patients by means of cortical-surface and transcortical recordings obtained during neurosurgery. 2. Contralateral stimulation evoked three groups of SEPs recorded from the hand representation area of sensorimotor cortex: P45-N80-P180, recorded anterior to the central sulcus (CS) and maximal on the precentral gyrus; N45-P80-N180, recorded posterior to the CS and maximal on the postcentral gyrus; and P50-N90-P190, recorded near and on either side of the CS. 3. P45-N80-P180 inverted in polarity to N45-P80-N180 across the CS but was similar in polarity from the cortical surface and white matter in transcortical recordings. These spatial distributions were similar to those of the short-latency P20-N30 and N20-P30 potentials described in the preceding paper, suggesting that these long-latency potentials are generated in area 3b of somatosensory cortex. 4. P50-N90-P190 was largest over the anterior one-half of somatosensory cortex and did not show polarity inversion across the CS. This spatial distribution was similar to that of the short-latency P25-N35 potentials described in the preceding paper and, together with our and Goldring et al. 1970; Stohr and Goldring 1969 transcortical recordings, suggest that these long-latency potentials are generated in area 1 of somatosensory cortex. 5. SEPs of apparently local origin were recorded from several regions of sensorimotor cortex to stimulation of the ipsilateral median nerve. Surface and transcortical recordings suggest that the ipsilateral potentials are generated not in area 3b, but rather in other regions of sensorimotor cortex perhaps including areas 4, 1, 2, and 7. This spatial distribution suggests that the ipsilateral potentials are generated by transcallosal input from the contralateral hemisphere. 6. Recordings from the periSylvian region were characterized by P100 and N100, recorded above and below the Sylvian sulcus (SS) respectively. This distribution suggests a tangential generator located in the upper wall of the SS in the second somatosensory area (SII). In addition, N125 and P200, recorded near and on either side of the SS, suggest a radial generator in a portion of SII located in surface cortex above the SS. 7. In comparison with the short-latency SEPs described in the preceding paper, the long-latency potentials were more variable and were more affected by intraoperative conditions.


2014 ◽  
Vol 111 (12) ◽  
pp. 2544-2553 ◽  
Author(s):  
Ephrem T. Zewdie ◽  
Francois D. Roy ◽  
Yoshino Okuma ◽  
Jaynie F. Yang ◽  
Monica A. Gorassini

Inhibitory feedback from sensory pathways is important for controlling movement. Here, we characterize, for the first time, a long-latency, inhibitory spinal pathway to ankle flexors that is activated by low-threshold homonymous afferents. To examine this inhibitory pathway in uninjured, healthy participants, we suppressed motor-evoked potentials (MEPs), produced in the tibialis anterior (TA), by a prior stimulation to the homonymous common peroneal nerve (CPN). The TA MEP was suppressed by a triple-pulse stimulation to the CPN, applied 40, 50, and 60 ms earlier and at intensities of 0.5–0.7 times motor threshold (average suppression of test MEP was 33%). Whereas the triple-pulse stimulation was below M-wave and H-reflex threshold, it produced a long-latency inhibition of background muscle activity, approximately 65–115 ms after the CPN stimulation, a time period that overlapped with the test MEP. However, not all of the MEP suppression could be accounted for by this decrease in background muscle activity. Evoked responses from direct activation of the corticospinal tract, at the level of the brain stem or thoracic spinal cord, were also suppressed by low-threshold CPN stimulation. Our findings suggest that low-threshold muscle and cutaneous afferents from the CPN activate a long-latency, homonymous spinal inhibitory pathway to TA motoneurons. We propose that inhibitory feedback from spinal networks, activated by low-threshold homonymous afferents, helps regulate the activation of flexor motoneurons by the corticospinal tract.


Sign in / Sign up

Export Citation Format

Share Document