Vengateswaran J. Ravichandran

Interactions Between Limb and Environmental Mechanics Influence Stretch Reflex Sensitivity in the Human Arm

Stretch reflexes contribute to arm impedance and longer-latency stretch reflexes exhibit increased sensitivity during interactions with compliant or unstable environments. This increased sensitivity is consistent with a regulation of arm impedance to compensate for decreased stability of the environment, but the specificity of this modulation has yet to be investigated. Many tasks, such as tool use, compromise arm stability along specific directions, and stretch reflexes tuned to those directions could present an efficient mechanism for regulating arm impedance in a task-appropriate manner. To be effective, such tuning should adapt not only to the mechanical properties of the environment but to those properties in relation to the arm, which also has directionally specific mechanical properties. The purpose of this study was to investigate the specificity of stretch reflex modulation during interactions with mechanical environments that challenge arm stability. The tested environments were unstable, having the characteristics of a negative stiffness spring. These were either aligned or orthogonal to the direction of maximal endpoint stiffness for each subject. Our results demonstrate preferential increases in reflexes, elicited within 50-100 ms of perturbation onset, to perturbations applied specifically along the direction of the destabilizing environments. This increase occurred only when the magnitude of the environmental instability exceeded endpoint stiffness along the same direction. These results are consistent with task-specific reflex modulation tuned to the mechanical properties of the environment relative to those of the human arm. They demonstrate a highly adaptable, involuntary mechanism that may be used to modulate limb impedance along specific directions.

Altered multijoint reflex coordination is indicative of motor impairment level following stroke

Following stroke, individuals often are unable to activate their elbow and shoulder muscles independently. There is growing evidence that altered reflex pathways may contribute to these abnormal patterns of activation or muscle synergies. Most studies investigating reflex function following stroke have examined only individual joints at rest. Thus, the purpose of this study was to quantify multijoint reflex contributions to the stereotyped muscle synergies commonly observed following stroke. We hypothesized that the patterns of reflex coordination mirror the abnormal muscle coactivity patterns previously reported for voluntary activation. 10 chronic stroke and 8 age-matched control subjects participated. Reflexes were elicited by perturbing the arm with a 3 degree of freedom robot while subjects exerted voluntary forces at the elbow and shoulder. The force conditions tested were selected to assess the influence of gravity and the influence of joint torque generation without gravity on reflex coordination. Reflex magnitude was quantified by the average rectified electromyogram, recorded from 8 muscles that span the elbow and shoulder. Patterns of reflex coordination were quantified using independent components analysis. Results show significant reflex coupling between elbow flexor and shoulder abductor-extensor muscles in stroke patients during isolated elbow and shoulder torque generation and during active arm support against gravity. Identified patterns of stretch reflex coordination were consistent with the stereotyped voluntary flexion synergy, suggesting reflex pathways contribute to abnormal muscle coordination following stroke.

Mechanical perturbations applied during impending movement evoke startle-like responses

Stretch reflexes have been considered one of the simplest circuits in the human nervous system. Yet, their role is controversial given that they assist or resist an imposed perturbation depending on the task instruction. Evidence shows that a loud acoustic stimulus applied prior to an impending movement elicits a movement-direction dependent muscle activity. In our study, we found that a perturbation can also trigger this early onset of movement, if applied during movement preparation. These responses were also perturbation direction dependent. This suggests an interaction of between the limb-stabilizing stretch reflexes and the voluntary activity.

Nonparametric identification of the elbow joint stiffness under compliant loads

Several nonparametric system identification techniques have been used to estimate the dynamic joint stiffness of the human elbow. Most studies involved a very stiff environment, but some studies have also shown that stiffness is modified in response to environmental compliance. However, using the same identification technique used under very stiff conditions to do identification under compliant conditions leads to a biased estimate. This is due to the presence of feedback in the latter. In this paper, we use a nonparametric identification algorithm to demonstrate this problem. We then show how instrumental variables can be employed to obtain an unbiased estimate of the same. Both simulations as well as experimental data are used to this effect.

Evidence for startle as a measurable behavioral indicator of motor learning

The ability of the classic startle reflex to evoke voluntarily prepared movement involuntarily has captured the attention of neuroscientists for its wide-ranging functional utility and potential uses in patient populations. To date, there is only one documented task resistant to the startReact phenomenon–index finger abduction. Previous reports have suggested the lack of startReact is due to different neural mechanisms driving individuated finger movement and more proximal joint control (e.g. elbow, wrist movement). However, an alternative hypothesis exists. Though not particularly difficult to execute, isolated index finger abduction is rarely performed during activities of daily living and is not a natural correlate to common individuated finger tasks. We propose that startReact can be evoked during individuated finger movements but only during tasks that are highly trained or familiar. The objective of this study was to determine the impact of a 2-week training regimen on the ability to elicit startReact. We found evidence in support of our hypothesis that following training, individuated movements of the hands (specifically index finger abduction) become susceptible to startReact. This is significant not only because it indicates that individuated finger movements are in fact amenable to startReact, but also that startle has differential response characteristics in novel tasks compared to highly trained tasks suggesting that startle is a measurable behavioral indicator of motor learning.

Reflex modulation is linked to the orientation of arm mechanics relative to the environment

To successfully complete a motor task, it is necessary to control not only the kinematics and dynamics of a limb, but also its mechanical properties. In a multijoint task such as the control of arm posture, limb mechanics are directional, resisting external disturbances more effectively in certain directions than others. It has been demonstrated that feedforward neuromotor pathways can regulate these directional characteristics of the arm to compensate for changes in the mechanical properties of the environment. However, it is unclear if spinal reflex pathways exhibit a similar specificity. The present results suggest that the sensitivity of the human stretch reflex also can be tuned to adapt the mechanical properties of the arm in a task appropriate manner. We hypothesized that the orientation of arm mechanics relative to the mechanical properties of the environment would influence reflex adaptation. Two destabilizing environments, oriented relative to the mechanical properties of the arm, were used to test this hypothesis. These environments were simulated using a 3 degrees of freedom (DOF) robot, which also was used to perturb arm posture. The resulting reflexes, assessed by electromyograms recorded from 8 muscles, were found to modulate in accordance with how the environmental instability was oriented relative to the mechanical properties of the arm. Our results suggest that stretch sensitive reflexes throughout the arm are modulated in a coordinated manner corresponding to the orientation of arm mechanics relative to the environment.

The influence of startReact on long-latency reflexive muscle activation during the transition from posture to movement

Many motor tasks involve transitions from posture to movement such as shifting from holding an object to setting it on a surface. Although many movements are voluntary processes, they are facilitated through motor pathways that span the continuum between reflexive and voluntary control. The mechanisms driving the long-latency stretch reflex (LLSR) have remained hotly contested. Recently, startReact has been shown to influence the fast muscular response to perturbations (Ravichandran et. al. 2013). The objective of this study was to evaluate how the LLSR and startReact impact the muscular response during the transition from posture to movement. We hypothesized that both the LLSR and startReact would be involved throughout the transition from posture to movement; however there would be a clear transition from LLSR dominance during posture to startReact dominance near/during movement. We tested this hypothesis using perturbations of elbow posture at various times before a fast ballistic extension movement. We found clear evidence that both the LLSR and startReact components were influenced changes in the late long-latency time window. The results provide insights on how the nervous system regulates involuntary responses to perturbations during the transition from maintenance of arm posture to movement. New and Noteworthy We recently demonstrated that the startReact effect, the startled release of a planned movement, can influence the muscular response during the LLSR. Here we observe how the influence of startReact can change from the transition from posture (no/little influence) to movement (strong influence). While not all paradigms trigger a startReact effect, this work demonstrates that when present startRect can have a profound effect on the overall muscle activity - even obscuring the traditional LLSR response.

Estimation of muscle synergies in the presence of arbitrary inputs

The strategy the central nervous system utilizes to produce movements in the face of multiple degrees of freedom available has been a subject of study for the past few years. Of the possible mechanisms, the muscle synergies-stereotypical coordinated patterns of muscle activity elicited by dedicated networks have been suggested to be the building blocks. Based on this hypothesis, several algorithms have been proposed to discern these synergies from the recorded electromyographic signals (EMG). In the proposed model, the synergies are treated as filters (IRFs) that take as input any arbitrary non-negative signal. That is, the EMG is seen as a convolution mixture of synergies and corresponding inputs.

Startle evokes nearly identical movements in multi-jointed, two-dimensional reaching tasks

StartReact is the ability of the startle reflex to involuntarily release a planned movement in the presence of a loud acoustic stimulus resulting in muscle activity patterns and kinematics that are tightly regulated and scaled with the intended action. Previous studies demonstrated startReact’s robustness during simple single-joint reaching tasks and found no difference between startReact and voluntary movements for movement kinematics and muscle activation patterns. However, startReact has not been evaluated during multi-joint reaching movements with multiple degrees of freedom. It is unclear if startReact would evoke accurate and precise multi-joint reaching movements in an unrestricted workspace. Furthermore, if tested more rigorously, multi-joint startReact movement kinematics and muscle activation patterns might not be truly equivalent despite showing no difference through traditional ANOVAs. A previous study found multi-joint startReact was possible during unrestricted elbow and shoulder movement when reaching to a forward target. Therefore, we hypothesized that startReact would evoke similar multi-joint reaching movements for movement accuracy and muscle activation patterns when compared to voluntary movements in a multi-directional workspace. Expanding upon the previous study, our study uses a larger workspace and fully evaluates movement kinematics and muscle activations patterns. Results confirmed our hypothesis and found startReact movements were readily evoked in all directions. StartReact responses presented stereotypically earlier muscle activation, but the relative timing of agonist/antagonist firing pairs between startReact and voluntary movements remained similar. Results demonstrate that startReact is robustly present and equivalent in multi-joint reaching tasks and has potential clinical use for evaluating healthy and impaired movement.

Muscle contributions to limb stiffness and stability in three dimensions

Successful task completion requires strength to counter external forces acting on a limb and stability to maintain limb posture. However, these simultaneous requirements can be at odds with each other as reaction forces directed towards the joints can interact with limb geometry to reduce limb stability. Net stability is due to these external force effects combined with the stability provided by muscles resisting those forces. The goal of this study was to quantify the contributions of cat hindlimb muscles to the 3D force generation and stability properties of the entire limb. Our hypothesis is that anti-gravity extensors must be co-activated with flexors to counter the destabilizing effects of the ground reaction forces directed towards the joints. Data were collected during three experimental conditions: passive, electrical stimulation of the triceps surae on its own, and in conjunction with the hamstrings. We found that the hamstrings muscle group, a leg extensor, destabilized hindlimb posture. These instabilities could be countered by simultaneous co-contraction of the triceps surae muscle group, which had a net ground reaction force in flexion direction. These initial results support our hypothesis that muscles generating downward forces (leg extensors) decrease limb stability.