Influence of kinesthetic motor imagery and effector specificity on the long-latency stretch response

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.

Stabilizing stretch reflexes are modulated independently from the rapid release of perturbation-triggered motor plans

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.

Lower Extremity Long-Latency Reflexes Differentiate Walking Function After Stroke

The neural mechanisms of walking impairment after stroke are not well characterized. There is a need for a neurophysiologic marker that can unambiguously differentiate functional status and potential for walking recovery. The long-latency reflex (LLR) is a supraspinally-mediated response that integrates sensorimotor information during movement. It is hypothesized that lower extremity LLRs contribute to regulation of motor output during walking in healthy individuals. The goal of the present study was to assess the relationship between lower extremity LLRs, measures of supraspinal drive, and walking function. Thirteen individuals with chronic post-stroke hemiparesis and thirteen healthy controls performed both isometric and dynamic plantarflexion. Transcranial magnetic stimulation (TMS) assessed supraspinal drive to the tibialis anterior. LLR activity was assessed during dynamic voluntary plantarflexion and individuals post-stroke were classified as either LLR present (LLR+) or absent (LLR-). All healthy controls and nine individuals post-stroke exhibited LLRs, while four did not. LLR+ individuals revealed higher clinical scores, walking speeds, and greater ankle plantarflexor power during walking compared to LLR- individuals. LLR- individuals exhibited exaggerated responses to TMS during dynamic plantarflexion relative to healthy controls. This LLR- subset revealed dysfunctional modulation of stretch responses and antagonist supraspinal drive relative to healthy controls and the higher functioning LLR+ individuals post-stroke. These abnormal responses allow for unambiguous differentiation between individuals post-stroke and are associated with multiple measures of motor function. These findings provide an opportunity to distinguish among the heterogeneity of lower extremity motor impairments present following stroke by associating them with responses at the nervous system level.

Long-latency reflexes for inter-effector coordination reflect a continuous state feedback controller

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.

Voluntary reaction time and long-latency reflex modulation

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.