Influence of environmental stability on the regulation of end-point impedance during the maintenance of arm posture.

Many common tasks compromise arm stability along specific directions. Such tasks can be completed only if the impedance of the arm is sufficient to compensate for the destabilizing effects of the task. During movement, it has been demonstrated that the direction of maximal arm stiffness, the static component of impedance, can be preferentially increased to compensate for directionally unstable environments. In contrast, numerous studies have shown that such control is not possible during postural tasks. It remains unknown if these findings represent a fundamental difference in the control of arm mechanics during posture and movement or an involuntary response to the destabilizing environments used in the movement studies but not yet tested during posture maintenance. Our goal was to quantify how arm impedance is adapted during postural tasks that compromise stability along specific directions. Our results demonstrate that impedance can be modulated to compensate for these instabilities during postural tasks but that the changes are modest relative to those previously reported during reaching. Our observed changes were primarily in the magnitude of end-point stiffness, but these were not sufficient to alter the direction of maximal stiffness. Furthermore, there were no substantial changes in the magnitude of end-point viscosity or inertia, suggesting that the primary change to arm impedance was a selective increase in stiffness to compensate for the destabilizing stiffness properties of the environment. We suggest that these modest changes provide an initial involuntary response to destabilizing environments prior to the larger changes that can be affected through voluntary interventions.

Contributions of altered stretch reflex coordination to arm impairments following stroke.

Patterns of stereotyped muscle coactivation, clinically referred to as synergies, emerge following stroke and impair arm function. Although researchers have focused on cortical contributions, there is growing evidence that altered stretch reflex pathways may also contribute to impairment. However, most previous reflex studies have focused on passive, single-joint movements without regard to their coordination during volitional actions. The purpose of this study was to examine the effects of stroke on coordinated activity of stretch reflexes elicited in multiple arm muscles following multijoint perturbations. We hypothesized that cortical injury results in increased stretch reflexes of muscles characteristic of the abnormal flexor synergy during active arm conditions. To test this hypothesis, we used a robot to apply position perturbations to impaired arms of 10 stroke survivors and dominant arms of 8 healthy age-matched controls. Corresponding reflexes were assessed during volitional contractions simulating different levels of gravitational support, as well as during voluntary flexion and extension of the elbow and shoulder. Reflexes were quantified by average rectified surface electromyogram, recorded from eight muscles spanning the elbow and shoulder. Reflex coordination was quantified using an independent components analysis. We found stretch reflexes elicited in the stroke group were significantly less sensitive to changes in background muscle activation compared with those in the control group (P < 0.05). We also observed significantly increased reflex coupling between elbow flexor and shoulder abductor-extensor muscles in stroke subjects relative to that in control subjects. This increased coupling was present only during volitional tasks that required elbow flexion (P < 0.001), shoulder extension (P < 0.01), and gravity opposition (P < 0.01), but not during the "no load" condition. During volitional contractions, reflex amplitudes scaled with the level of impairment, as assessed by Fugl-Meyer scores (r(2) = 0.63; P < 0.05). We conclude that altered reflex coordination is indicative of motor impairment level and may contribute to impaired arm function following stroke.

Stretch sensitive reflexes as an adaptive mechanism for maintaining limb stability.

The often studied stretch reflex is fundamental to the involuntary control of posture and movement. Nevertheless, there remains controversy regarding its functional role. Many studies have demonstrated that stretch reflexes can be modulated in a task appropriate manner. This review focuses on modulation of the long-latency stretch reflex, thought to be mediated, at least in part, by supraspinal pathways. For example, this component of the stretch reflex increases in magnitude during interactions with compliant environments, relative to its sensitivity during interactions with rigid environments. This suggests that reflex sensitivity increases to augment limb stability when that stability is not provided by the environment. However, not all results support the stabilizing role of stretch reflexes. Some studies have demonstrated that involuntary responses within the time period corresponding to the long-latency reflex can destabilize limb posture. We propose that this debate stems from the fact that multiple perturbation-sensitive pathways can contribute to the long-latency stretch reflex and that these pathways have separate functional roles. The presented studies suggest that neural activity occurring within the period normally ascribed to the long-latency stretch reflex is highly adaptable to current task demands and possibly should be considered more intelligent than "reflexive".

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.

Effects of environmental instabilities on endpoint stiffness during the maintenance of human arm posture.

Using the upper limb to manipulate objects or tools requires maintenance of stable arm posture. The ability to maintain stable postures is dependent on the mechanical properties of the arm, which can be characterized by estimates of endpoint stiffness. In this study we quantified the endpoint stiffness of the human arm during postural interactions with mechanically imposed unstable loads. The purpose was to determine the extent to which arm stiffness is adapted according to the mechanical properties of the environment during postural tasks. We estimated the endpoint stiffness of the right arms of eight subjects as they interacted with four haptic environments: rigid, unstable along the direction of maximal endpoint stiffness and orthogonal to this direction, and a high-strength unstable environment also aligned to the orientation of maximal endpoint stiffness. The size and orientation of endpoint stiffness were quantified for each haptic condition. Stiffness size was increased along the directions of the destabilizing environments (p<0.003). However, the environments had no significant effect on stiffness orientation (p>0.26). These findings suggest that at a fixed posture interactions with unstable environments can induce moderate, task-appropriate changes in limb mechanics that are tuned to the environment. However, these changes are small relative to those that can be obtained by changing limb posture.

Use of self-selected postures to regulate multi-joint stiffness during unconstrained tasks.

BACKGROUND: The human motor system is highly redundant, having more kinematic degrees of freedom than necessary to complete a given task. Understanding how kinematic redundancies are utilized in different tasks remains a fundamental question in motor control. One possibility is that they can be used to tune the mechanical properties of a limb to the specific requirements of a task. For example, many tasks such as tool usage compromise arm stability along specific directions. These tasks only can be completed if the nervous system adapts the mechanical properties of the arm such that the arm, coupled to the tool, remains stable. The purpose of this study was to determine if posture selection is a critical component of endpoint stiffness regulation during unconstrained tasks. METHODOLOGY/PRINCIPAL FINDINGS: Three-dimensional (3D) estimates of endpoint stiffness were used to quantify limb mechanics. Most previous studies examining endpoint stiffness adaptation were completed in 2D using constrained postures to maintain a non-redundant mapping between joint angles and hand location. Our hypothesis was that during unconstrained conditions, subjects would select arm postures that matched endpoint stiffness to the functional requirements of the task. The hypothesis was tested during endpoint tracking tasks in which subjects interacted with unstable haptic environments, simulated using a 3D robotic manipulator. We found that arm posture had a significant effect on endpoint tracking accuracy and that subjects selected postures that improved tracking performance. For environments in which arm posture had a large effect on tracking accuracy, the self-selected postures oriented the direction of maximal endpoint stiffness towards the direction of the unstable haptic environment. CONCLUSIONS/SIGNIFICANCE: These results demonstrate how changes in arm posture can have a dramatic effect on task performance and suggest that postural selection is a fundamental mechanism by which kinematic redundancies can be exploited to regulate arm stiffness in unconstrained tasks.

The separate neural control of hand movements and contact forces.

To manipulate an object, we must simultaneously control the contact forces exerted on the object and the movements of our hand. Two alternative views for manipulation have been proposed: one in which motions and contact forces are represented and controlled by separate neural processes, and one in which motions and forces are controlled jointly, by a single process. To evaluate these alternatives, we designed three tasks in which subjects maintained a specified contact force while their hand was moved by a robotic manipulandum. The prescribed contact force and hand motions were selected in each task to induce the subject to attain one of three goals: (1) exerting a regulated contact force, (2) tracking the motion of the manipulandum, and (3) attaining both force and motion goals concurrently. By comparing subjects' performances in these three tasks, we found that behavior was captured by the summed actions of two independent control systems: one applying the desired force, and the other guiding the hand along the predicted path of the manipulandum. Furthermore, the application of transcranial magnetic stimulation impulses to the posterior parietal cortex selectively disrupted the control of motion but did not affect the regulation of static contact force. Together, these findings are consistent with the view that manipulation of objects is performed by independent brain control of hand motions and interaction forces.

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.

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.

Motor cortical measures of use-dependent plasticity are graded from distal to proximal in the human upper limb.

In humans, it is well established that practicing simple, repetitive movements with the distal upper limb induces short-term plasticity in the neural pathways that control training. It is unknown how the neural response to similar training at more proximal joints differs. The purpose of this study was to quantify how ballistic training at proximal and distal upper limb joints influences measures of corticomotor plasticity. To accomplish this goal, we had subjects repetitively practice simple movements for 30 min using the index finger, wrist, or elbow. Before and after training, transcranial magnetic stimulation (TMS) was used to activate the corticomotor pathways innervating the trained joint. We assessed the effect of training by quantifying changes in TMS-elicited joint movements and motor-evoked potentials in the training agonists and antagonists. These measures of training-induced neural plasticity were graded from distal to proximal in the upper limb. Training had the greatest immediate effect on the pathways controlling the index finger and this effect decreased for more proximal joints. Our results suggest that the relative sizes and properties of the cortical areas controlling the proximal and distal upper limb influence the effect of training on the corticomotor pathways. These results have implications for how training influences the neural pathways controlling movement in the proximal and distal portions of the human upper limb and the degree to which these effects can be quantified using TMS.