The long-latency reflex is composed of at least two functionally independent processes

2011 ◽  
Vol 106 (1) ◽  
pp. 449-459 ◽  
Author(s):  
J. Andrew Pruszynski ◽  
Isaac Kurtzer ◽  
Stephen H. Scott

The nervous system counters mechanical perturbations applied to the arm with a stereotypical sequence of muscle activity, starting with the short-latency stretch reflex and ending with a voluntary response. Occurring between these two events is the enigmatic long-latency reflex. Although researchers have been fascinated by the long-latency reflex for over 60 years, some of the most basic questions about this response remain unresolved and often debated. In the present study we help resolve one such question by providing clear evidence that the human long-latency reflex during a naturalistic motor task is not a single functional response; rather, it appears to reflect the output of (at least) two functionally independent processes that overlap in time and sum linearly. One of these functional components shares an important attribute of the short-latency reflex (i.e., automatic gain scaling, sensitivity to background load), and the other shares a defining feature of voluntary control (i.e., task dependency, sensitivity to goal target position). We further show that the task-dependent component of long-latency activity reflects a feedback control process rather than the simplest triggered reaction to a mechanical stimulus.

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Hyunglae Lee ◽  
Eric J. Perreault

Abstract Responses elicited after the shortest latency spinal reflexes but prior to the onset of voluntary activity can display sophistication beyond a stereotypical reflex. Two distinct behaviors have been identified for these rapid motor responses, often called long-latency reflexes. The first is to maintain limb stability by opposing external perturbations. The second is to quickly release motor actions planned prior to the disturbance, often called a triggered reaction. This study investigated their interaction when motor tasks involve both limb stabilization and motor planning. We used a robotic manipulator to change the stability of the haptic environment during 2D arm reaching tasks, and to apply perturbations that could elicit rapid motor responses. Stabilizing reflexes were modulated by the orientation of the haptic environment (field effect) whereas triggered reactions were modulated by the target to which subjects were instructed to reach (target effect). We observed that there were no significant interactions between the target and field effects in the early (50–75 ms) portion of the long-latency reflex, indicating that these components of the rapid motor response are initially controlled independently. There were small but significant interactions for two of the six relevant muscles in the later portion (75–100 ms) of the reflex response. In addition, the target effect was influenced by the direction of the perturbation used to elicit the motor response, indicating a later feedback correction in addition to the early component of the triggered reaction. Together, these results demonstrate how distinct components of the long-latency reflex can work independently and together to generate sophisticated rapid motor responses that integrate planning with reaction to uncertain conditions.


1985 ◽  
Vol 53 (5) ◽  
pp. 1179-1193 ◽  
Author(s):  
B. Calancie ◽  
P. Bawa

Single motor unit and gross surface electromyographic responses to torque motor-produced wrist extensions were studied in human flexor carpi radialis muscle. Surface EMG typically showed two "periods" of reflex activity, at a short and long latency following stretch, but both periods occurring before a subject's voluntary reaction to the stretch. The amplitude of EMG activity in both reflex periods increased monotonically with an increase in the torque load. The amplitude of the short-latency reflex response was very dependent on the motoneuron pool excitability, or preload. The amplitude of the long-latency reflex response also varied with the preload, but could, in addition, be modulated by the subject's preparatory set for a voluntary response to the imposed displacement. When a single motor unit that was not tonically active began to fire during the stretch reflex, it did so primarily during the long-latency period. When caused to fire repetitively by voluntary facilitation of the motoneuron pool, that same unit now showed activity during both periods of the stretch reflex. Further increases in either motoneuron pool facilitation or in perturbation strength resulted in a monotonic increase in response probability of a single motor unit during the short-latency period. However, the response probability of a single unit during the long-latency reflex period did not always vary in a monotonic way with increases in either torque load or motoneuron pool facilitation. For an additional series of experiments, the subject was instructed on how to respond voluntarily to the upcoming wrist perturbation. The three instructions to the subject had no effect on the response probability of a single motor unit during either the background or short-latency periods of the stretch reflex. However, prior instruction clearly affected a unit's response probability during the long-latency reflex period. Changes in the firing rate of motor units, and in the recruitment or derecruitment of nontonic units, contributed to this modulation of reflex activity during the long-latency period.


2015 ◽  
Vol 114 (6) ◽  
pp. 3386-3399 ◽  
Author(s):  
Christopher J. Forgaard ◽  
Ian M. Franks ◽  
Dana Maslovat ◽  
Laurence Chin ◽  
Romeo Chua

Stretching a muscle of the upper limb elicits short (M1) and long-latency (M2) reflexes. When the participant is instructed to actively compensate for a perturbation, M1 is usually unaffected and M2 increases in size and is followed by the voluntary response. It remains unclear if the observed increase in M2 is due to instruction-dependent gain modulation of the contributing reflex mechanism(s) or results from voluntary response superposition. The difficulty in delineating between these alternatives is due to the overlap between the voluntary response and the end of M2. The present study manipulated response accuracy and complexity to delay onset of the voluntary response and observed the corresponding influence on electromyographic activity during the M2 period. In all active conditions, M2 was larger compared with a passive condition where participants did not respond to the perturbation; moreover, these changes in M2 began early in the appearance of the response (∼50 ms), too early to be accounted for by voluntary overlap. Voluntary response latency influenced the latter portion of M2, with the largest activity seen when accuracy of limb position was not specified. However, when participants aimed for targets of different sizes or performed movements of various complexities, reaction time differences did not influence M2 period activity, suggesting voluntary activity was sufficiently delayed. Collectively, our results show that while a perturbation applied to the upper limbs can trigger a voluntary response at short latency (<100 ms), instruction-dependent reflex gain modulation remains an important contributor to EMG changes during the M2 period.


2008 ◽  
Vol 100 (1) ◽  
pp. 224-238 ◽  
Author(s):  
J. Andrew Pruszynski ◽  
Isaac Kurtzer ◽  
Stephen H. Scott

Considerable research has established that rapid motor responses (traditionally called reflexes), can be modified by a subject's voluntary goals. Here, we expand on past observations using verbal instructions by defining the voluntary goal via visual target position. This approach allowed us to objectively enforce task adherence and explore a richer set of variables, such as target direction and distance, metrics that modify voluntary control and that—according to our hypothesis—will influence rapid motor responses. Our first experiment tested whether upper-limb responses are categorically modulated by target direction by placing targets such that the same perturbation could push the hand into one target and out of the other, a spatial analogue to “resist/yield” verbal instructions. Consistent with these classical results, we found that the short-latency rapid response (R1, 20–45 ms) was not modulated by target direction, whereas long-latency rapid responses (R2/R3, 45–105 ms) were modified in a manner approaching the voluntary response (VOL, 120–180 ms). Our second experiment tested whether upper-limb responses are continuously modulated by target distance by distributing five targets along one axis centered on the hand. Here, the long-latency and voluntary response mirrored the task demands by increasing activity in a graded fashion with increasing target distance. Our final experiment explored how upper-limb responses incorporate two-dimensional spatial information by placing targets radially around the hand. Notably, long-latency responses exhibited smooth tuning functions to target direction that were similar to those observed for the voluntary response. Taken together, these results illustrate the flexibility of long-latency rapid responses and emphasize their similarity to later voluntary responses.


2019 ◽  
Vol 122 (5) ◽  
pp. 2187-2200 ◽  
Author(s):  
Christopher J. Forgaard ◽  
Ian M. Franks ◽  
Dana Maslovat ◽  
Romeo Chua

The long-latency “reflexive” response (LLR) following an upper limb mechanical perturbation is generated by neural circuitry shared with voluntary control. This feedback response supports many task-dependent behaviors and permits the expression of goal-directed corrections at latencies shorter than voluntary reaction time. An extensive body of literature has demonstrated that the LLR shows flexibility akin to voluntary control, but it has not yet been tested whether instruction-dependent LLR changes can also occur in the absence of an overt voluntary response. The present study used kinesthetic motor imagery ( experiment 1) and instructed participants to execute movement with the unperturbed contralateral limb ( experiment 2) to explore the relationship between the overt production of a voluntary response and LLR facilitation. Activity in stretched right wrist flexors were compared with standard “do not-intervene” and “compensate” conditions. Our findings revealed that on ~40% of imagery and ~50% of contralateral trials, a response occurred during the voluntary epoch in the stretched right wrist flexors. On these “leaked” trials, the early portion of the LLR (R2) was facilitated and displayed a similar increase to compensate trials. The latter half of the LLR (R3) showed further modulation, mirroring the patterns of voluntary epoch activity. By contrast, the LLR on “non-leaked” imagery and contralateral trials did not modulate. We suggest that even though a hastened voluntary response cannot account for all instruction-dependent LLR modulation, the overt execution of a response during the voluntary epoch in the same muscle(s) as the LLR is a prerequisite for instruction-dependent facilitation of this feedback response. NEW & NOTEWORTHY Using motor imagery and contralateral responses, we provide novel evidence that facilitation of the long-latency reflex (LLR) requires the execution of a response during the voluntary epoch. A high proportion of overt response “leaks” were found where the mentally simulated or mirrored response appeared in stretched muscle. The first half of the LLR was categorically sensitive to the appearance of leaks, whereas the latter half displayed characteristics closely resembling activity in the ensuing voluntary period.


2014 ◽  
Vol 111 (8) ◽  
pp. 1631-1645 ◽  
Author(s):  
Isaac Kurtzer ◽  
Frédéric Crevecoeur ◽  
Stephen H. Scott

Corrective muscle responses occurring 50–100 ms after a mechanical perturbation are tailored to the mechanical features of the limb and its environment. For example, the evoked response by the shoulder's extensor muscle counters an imposed shoulder torque, rather than local shoulder motion, by integrating motion information from the shoulder and elbow appropriate for their dynamic interaction. Previous studies suggest that arm muscle activity within this epoch, alternately termed the R2/3 response, or long-latency reflex, reflects the summed result of two distinct components: an activity-dependent component which scales with the background muscle activity, and a task-dependent component which scales with the required vigor of the behavioral task. Here we examine how the knowledge of limb dynamics expressed during the shoulder muscle's R2/3 epoch is related to these two functional components. Subjects countered torque steps applied to their shoulder and/or elbow under different conditions of background torque and target size to recruit the activity-dependent and task-dependent component in varying degrees. Experiment 1 involved four torque perturbations, two levels of background torques and two target sizes; this design revealed that both background torque and target size impacted the shoulder's R2/3 activity, indicative of knowledge of limb dynamics. Experiment 2 involved two perturbation torques, five levels of background torque and two target sizes; this design demonstrated that the two factors had an independent impact on the R2/3 activity indicative of knowledge of limb dynamics. We conclude that a sophisticated feature of upper limb feedback control reflects the summation of two processes having a common capability.


2018 ◽  
Vol 120 (5) ◽  
pp. 2466-2483 ◽  
Author(s):  
Frederic Crevecoeur ◽  
Isaac Kurtzer

Successful performance in many everyday tasks requires compensating unexpected mechanical disturbance to our limbs and body. The long-latency reflex plays an important role in this process because it is the fastest response to integrate sensory information across several effectors, like when linking the elbow and shoulder or the arm and body. Despite the dozens of studies on inter-effector long-latency reflexes, there has not been a comprehensive treatment of how these reveal the basic control organization that sets constraints on any candidate model of neural feedback control such as optimal feedback control. We considered three contrasting ways that controllers can be organized: multiple independent controllers vs. a multiple-input multiple-output (MIMO) controller, a continuous feedback controller vs. an intermittent feedback controller, and a direct MIMO controller vs. a state feedback controller. Following a primer on control theory and review of the relevant evidence, we conclude that continuous state feedback control best describes the organization of inter-effector coordination by the long-latency reflex.


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.


2019 ◽  
Author(s):  
Rodrigo S. Maeda ◽  
Paul L. Gribble ◽  
J. Andrew Pruszynski

AbstractPrevious work has demonstrated that when learning a new motor task, the nervous system modifies feedforward (ie. voluntary) motor commands and that such learning transfers to fast feedback (ie. reflex) responses evoked by mechanical perturbations. Here we show the inverse, that learning new feedback responses transfers to feedforward motor commands. Sixty human participants (34 females) used a robotic exoskeleton and either 1) received short duration mechanical perturbations (20 ms) that created pure elbow rotation or 2) generated self-initiated pure elbow rotations. They did so with the shoulder joint free to rotate (normal arm dynamics) or locked (altered arm dynamics) by the robotic manipulandum. With the shoulder unlocked, the perturbation evoked clear shoulder muscle activity in the long-latency stretch reflex epoch (50-100ms post-perturbation), as required for countering the imposed joint torques, but little muscle activity thereafter in the so-called voluntary response. After locking the shoulder joint, which alters the required joint torques to counter pure elbow rotation, we found a reliable reduction in the long-latency stretch reflex over many trials. This reduction transferred to feedforward control as we observed 1) a reduction in shoulder muscle activity during self-initiated pure elbow rotation trials and 2) kinematic errors (ie. aftereffects) in the direction predicted when failing to compensate for normal arm dynamics, even though participants never practiced self-initiated movements with the shoulder locked. Taken together, our work shows that transfer between feedforward and feedback control is bidirectional, furthering the notion that these processes share common neural circuits that underlie motor learning and transfer.


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