The Strategy of Human Movement Control and Teaching Motor Skills in Norm and Pathology.

The strategy used by the brain to organize human goal-directed movements is still debated. Here, I argue that without the knowledge of this strategy, teaching movement skills required in complex sports activities and for rehabilitation of motor disorders remains an art and can often result in inefficient techniques and misleading instructions. However, the leading joint hypothesis offers a solution to this problem. It suggests that the control strategy consists in rotation of a single ('leading') joint actively and using the biomechanical effect produced by the leading joint as the primary contributor to motion of the other ('trailing') joints. This "trailing joint control pattern" was found in a large variety of movement types. This pattern is simple even for seemingly complex movements, it can be easily verbalized, and it requires focusing attention during learning only on one or two movement elements at a time. The use of the trailing joint control strategy therefore allows development of better targeted techniques of motor learning and rehabilitation.

Control of paretic and non-paretic upper extremity during bimanual reaching after stroke.

Most actions of daily life engage the two upper extremities (UEs) in a highly coordinated manner. While it is recognized that bimanual movements are impaired post-stroke, understanding how the paretic and non-paretic UE contributes to this impairment is important for future interventions. We investigated kinetic and kinematics at the shoulder, elbow, and wrist joints in the paretic and non-paretic UE in 8 individuals with chronic stroke and non-dominant UE in 8 healthy controls during unimanual and bimanual tasks. Kinematic analysis revealed little effect of stroke. However, kinetic analysis revealed that during unimanual movements, joint control was impaired during unimanual and bimanual movements in both UEs, although to a lesser extent in the non-paretic than paretic UE. During bimanual movements, joint control did not change in the paretic UE, and it further deteriorated in the non-paretic UE compared with the unimanual movements. Our findings suggest that a single session of bimanual task performance does not improve joint control of the paretic UE and it impairs control of the non-paretic UE, making it more like that of the paretic UE.

A simple joint control pattern dominates performance of unconstrained arm movements of daily living tasks.

A trailing joint control pattern, during which a single joint is rotated actively and the mechanical effect of this motion is used to move the other joints, was previously observed during simplified, laboratory-based tasks. We examined whether this simple pattern also underlies control of complex, unconstrained arm movements of daily activities. Six tasks were analyzed. Using kinematic data, we estimated motion of 7 degrees of freedom (DOF) of the shoulder, elbow, and wrist, and the contribution of muscle and passive interaction and gravitational torques to net torque at each joint. Despite task variety, the hand was transported predominantly by shoulder and elbow flexion/extension, although shoulder external/internal rotation also contributed in some tasks. The other DOF were used to orient the hand in space. The trailing pattern represented by production of net torque by passive torques at the shoulder or elbow or both was observed during the biggest portion of each movement. Net torque generation by muscle torque at both joints simultaneously was mainly limited to movement initiation toward the targets and movement termination when returning to the initial position, and associated with needing to overcome gravity. The results support the interpretation of previous studies that prevalence of the trailing pattern is a feature of skillful, coordinated movements. The simplicity of the trailing pattern is promising for quantification of dyscoordination caused by motor disorders and formulation of straightforward instructions to facilitate rehabilitation and motor learning.

Generalization of the resource-rationality principle to neural control of goal-directed movements.

We review evidence that the resource-rationality principle generalizes to human movement control. Optimization of the use of limited neurocomputational resources is described by the inclusion of the "neurocomputational cost" of sensory information processing and decision making in the optimality criterion of movement control. A resulting tendency to decrease this cost can account for various phenomena observed during goal-directed movements.

Effect of Stroke on Joint Control during Reach-to-Grasp: A Preliminary Study.

We investigated changes in control of inter-segmental dynamics underlying upper extremity dyscoordination caused by stroke. Individuals with stroke and healthy individuals performed a natural reach-to-grasp movement. Kinetic analysis revealed that both groups rotated the shoulder by muscle torque and used interaction torque to rotate the elbow. However, individuals with stroke used interaction torque less than healthy individuals, actively suppressing a substantial portion of it. This resulted in inefficient use of active control and dyscoordination of the upper extremity. The degree of interaction torque suppression and inefficiency of active control at the elbow positively correlated with stroke severity. The increased interaction torque suppression can be a strategy used by individuals with stroke to compensate for deficient feedforward control of this torque.

The role of intersegmental dynamics in coordination of the forelimb joints during unperturbed and perturbed skilled locomotion.

Joint coordination during locomotion and how this coordination changes in response to perturbations remains poorly understood. We investigated coordination among forelimb joints during the swing phase of skilled locomotion in the cat. While cats walked on a horizontal ladder, one of the cross-pieces moved before the cat reached it, requiring the cat to alter step size. Direction and timing of the cross-piece displacement were manipulated. We found that the paw was transported in space through body translation and shoulder and elbow rotations, whereas the wrist provided paw orientation required to step on cross-pieces. Kinetic analysis revealed a consistent joint control pattern in all conditions. Although passive interaction and gravitational torques were the main sources of shoulder and elbow motions for most of the movement time, shoulder muscle torque influenced movement of the entire limb at the end of the swing phase, accelerating the shoulder and causing interaction torque that determined elbow motion. At the wrist, muscle and passive torques predominantly compensated for each other. In all perturbed conditions, although all joints and the body slightly contributed to changes in the step length throughout the entire movement, the major adjustment was produced by the shoulder at the movement end. We conclude that joint coordination during the swing phase is produced mainly passively, by exploiting gravity and the limb's intersegmental dynamics, which may simplify the neural control of locomotion. The use of shoulder musculature at the movement end enables flexible responses to environmental disturbances. NEW & NOTEWORTHY This is the first study to investigate joint control during the swing phase of skilled, accuracy-dependent locomotion in the cat and how this control is altered to adapt to known and unexpected perturbations. We demonstrate that a pattern of joint control that exploits gravitational and interaction torques is used in all conditions and that movement modifications are produced mainly by shoulder muscle torque during the last portion of the movement.

Inclusion of neural effort in cost function can explain perceptual decision suboptimality.

A more general form of optimality approach applied to the entire behavioral paradigm should be used instead of abandoning the optimality approach. Adding the cost of information processing to the optimality criterion and taking into account some other recently proposed aspects of decision optimization could substantially increase the explanatory power of an optimality approach to modeling perceptual decision making.

Destabilization of the Upright Posture Through Elevation of the Center of Mass.

The inverted pendulum model predicts that the major challenge for neural control of the upright posture is the inherent instability of the body due to the center of mass (COM) being above the base of support (BOS). If so, even slight elevation of the COM may substantially destabilize posture. The destabilizing effect of heavy load positioned above the COM has been demonstrated. We examined sensitivity of posture to light (1-5% of body weight) load by placing weights on the shoulders and assessing functional reach distance in the forward, right, and left directions and postural sway during quiet stance. At each load level, the quiet stance task was tested with and without vision. The 1% of body weight load significantly shortened reach distance in the forward direction. It also increased postural sway. Interestingly, additional weight did not result in further deficits. The results support high sensitivity of postural stability to COM elevation that increases the challenge for neural control of posture and that can potentially be used for early detection of declines in postural stability.

Neural control of arm movements reveals a tendency to use gravity to simplify joint coordination rather than to decrease muscle effort.

How gravity influences neural control of arm movements remains under debate. We tested three alternative interpretations suggested by previous research: (1) that muscular control includes two components, tonic which compensates for gravity and phasic which produces the movement; (2) that there is a tendency to exploit gravity to reduce muscle effort; and (3) that there is a tendency to use a trailing pattern of joint control during which either the shoulder or elbow is rotated actively and the other joint rotates predominantly passively, and to exploit gravity for control of the passively rotated joint. A free-stroke drawing task was performed that required production of center-out strokes within a circle while selecting stroke directions randomly. The circle was positioned in the horizontal, sagittal, and frontal plane. The arm joints freely rotated in space. In each plane, the distribution of the strokes across directions was non-uniform. Directional histograms were built and their peaks were used to identify preferred movement directions. The directional preferences were especially pronounced in the two vertical planes. The upward directions were most preferred. To test the three interpretations, we used a kinetic analysis that determined the role of gravitational torque in the production of movement in the preferred directions. The results supported the third interpretation and provided evidence against the first and second interpretation. The trailing pattern has been associated with reduced neural effort for joint coordination, and therefore, we conclude that the major tendency with respect to gravity is to exploit it for simplification of joint coordination.

Strategy of arm movement control is determined by minimization of neural effort for joint coordination.

Optimality criteria underlying organization of arm movements are often validated by testing their ability to adequately predict hand trajectories. However, kinematic redundancy of the arm allows production of the same hand trajectory through different joint coordination patterns. We therefore consider movement optimality at the level of joint coordination patterns. A review of studies of multi-joint movement control suggests that a 'trailing' pattern of joint control is consistently observed during which a single ('leading') joint is rotated actively and interaction torque produced by this joint is the primary contributor to the motion of the other ('trailing') joints. A tendency to use the trailing pattern whenever the kinematic redundancy is sufficient and increased utilization of this pattern during skillful movements suggests optimality of the trailing pattern. The goal of this study is to determine the cost function minimization of which predicts the trailing pattern. We show that extensive experimental testing of many known cost functions cannot successfully explain optimality of the trailing pattern. We therefore propose a novel cost function that represents neural effort for joint coordination. That effort is quantified as the cost of neural information processing required for joint coordination. We show that a tendency to reduce this 'neurocomputational' cost predicts the trailing pattern and that the theoretically developed predictions fully agree with the experimental findings on control of multi-joint movements. Implications for future research of the suggested interpretation of the trailing joint control pattern and the theory of joint coordination underlying it are discussed.

Influence of workspace constraints on directional preferences of 3D arm movements.

We previously demonstrated a tendency to perform arm movements by using a trailing joint control pattern during which either the shoulder or elbow is rotated actively and the other (trailing) joint is rotated predominantly passively, by interaction torque during horizontal movements and by interaction and gravitational torque during 3D arm movements. This tendency was established with a free-stroke drawing task that required production of series of strokes in randomly selected directions from the center to the perimeter of a horizontal circle. The studies demonstrated that within a planar workspace, the usage of the trailing pattern depends on movement direction and the most frequently selected directions are those providing the opportunity to use the trailing pattern. Here, we studied whether the opportunity to use the preferred trailing pattern also depends on the orientation of the planar workspace. The free-stroke drawing task was performed with unconstrained arm movements within circles of a left-diagonal (LD) and right-diagonal (RD) orientation. Two pronounced preferred directions were revealed in the LD condition, and they were the directions in which the trailing pattern was used. Directional preferences were less pronounced, and the trailing pattern was not observed in any directions in the RD condition. Also, subjects identified the RD condition as inconvenient. The results reinforce the previous finding of the propensity to use the trailing pattern during arm movements. They also suggest that orientations of the workspaces in manual activities should be designed to support the trailing pattern as a favored type of joint control.

A preferred pattern of joint coordination during arm movements with redundant degrees of freedom.

Redundancy of degrees of freedom (DOFs) during natural human movements is a central problem of motor control research. This study tests a novel interpretation that during arm movements, the DOF redundancy is used to support a preferred, simplified joint control pattern that consists of rotating either the shoulder or elbow actively and the other (trailing) joint predominantly passively by interaction and gravitational torques. We previously revealed the preference for this control pattern during nonredundant horizontal arm movements. Here, we studied whether this preference persists during movements with redundant DOFs and the redundancy is used to enlarge the range of directions in which this control pattern can be utilized. A free-stroke drawing task was performed that involved production of series of horizontal center-out strokes in randomly selected directions. Two conditions were used, with the arm's joints unconstrained (U) and constrained (C) to the horizontal plane. In both conditions, directional preferences were revealed and the simplified control pattern was used in the preferred and not in nonpreferred directions. The directional preferences were weaker and the range of preferred directions was wider in the U condition, with higher percentage of strokes performed with the simplified control pattern. This advantage was related to the usage of additional DOFs. We discuss that the simplified pattern may represent a feedforward control strategy that reduces the challenge of joint coordination caused by signal-dependent noise during movement execution. The results suggest a possibility that the simplified pattern is used during the majority of natural, seemingly complex arm movements.

Intersegmental dynamics shape joint coordination during catching in typically developing children but not in children with developmental coordination disorder.

Factors shaping joint coordination during multijoint movements were studied using a one-handed ball-catching task. Typically developing (TD) boys between 9 and 12 yr of age, at which catching becomes consistently successful, and boys with developmental coordination disorder (DCD) of the same age participated in the study. The arm was initially stretched down. Catching was performed by flexing the shoulder and elbow and extending the wrist in the parasagittal plane. Catching success rate was substantially lower in children with DCD. Amplitudes and directions of joint motions were similar in both groups. Group differences were found in shoulder and elbow coordination patterns. TD children performed the movement predominantly by actively accelerating into flexion, one joint at a time-first the elbow and then the shoulder-and allowing passive interaction torque (IT) to accelerate the other joint into extension. Children with DCD tended to accelerate both joints into flexion simultaneously, suppressing IT. The results suggest that the TD joint coordination was shaped by the tendency to minimize active control of IT despite the complexity of the emergent joint kinematics. The inefficient control of IT in children with DCD points to deficiency of the internal model of intersegmental dynamics. Together, the findings advocate that joint coordination throughout a multijoint movement is a by-product of the control strategy that benefits from movement dynamics by actively accelerating a single joint and using IT for rotation of the other joint. Reduction of control-dependent noise is discussed as a possible advantage of this control strategy.

Preferred directions of arm movements are independent of visual perception of spatial directions.

Directional preferences have previously been demonstrated during horizontal arm movements. These preferences were characterized by a tendency to exploit interaction torques for movement production at the shoulder or elbow, indicating that the preferred directions depend on biomechanical, and not on visual perception-based factors. We directly tested this hypothesis by systematically dissociating visual information from arm biomechanics. Sixteen subjects performed a free-stroke drawing task that required performance of fast strokes from the circle center toward the perimeter, while selecting stroke directions in a random order. Hand position was represented by a cursor displayed in the movement plane. The free-stroke drawing was performed twice, before and after visuomotor adaptation to a 30° clockwise rotation of the perceived hand path. The adaptation was achieved during practicing pointing movements to eight center-out targets. Directional preferences during performance of the free-stroke drawing task were revealed in ten out of the sixteen subjects. The orientation and strength of these preferences were largely the same in both conditions, showing no significant effect of the visuomotor adaptation. In both conditions, the major preferred directions were characterized by higher contribution of interaction torque to net torque at the shoulder as well as by relatively low inertial resistance and the sum of squared shoulder and elbow muscle torques. These results support the hypothesis that directional preferences are largely determined by biomechanical factors. However, this biomechanical effect can decrease or even disappear in some subjects when movements are performed in special conditions, such as the virtual environment used here.

Load emphasizes muscle effort minimization during selection of arm movement direction.

BACKGROUND: Directional preferences during center-out horizontal shoulder-elbow movements were previously established for both the dominant and non-dominant arm with the use of a free-stroke drawing task that required random selection of movement directions. While the preferred directions were mirror-symmetrical in both arms, they were attributed to a tendency specific for the dominant arm to simplify control of interaction torque by actively accelerating one joint and producing largely passive motion at the other joint. No conclusive evidence has been obtained in support of muscle effort minimization as a contributing factor to the directional preferences. Here, we tested whether distal load changes directional preferences, making the influence of muscle effort minimization on the selection of movement direction more apparent. METHODS: The free-stroke drawing task was performed by the dominant and non-dominant arm with no load and with 0.454 kg load at the wrist. Motion of each arm was limited to rotation of the shoulder and elbow in the horizontal plane. Directional histograms of strokes produced by the fingertip were calculated to assess directional preferences in each arm and load condition. Possible causes for directional preferences were further investigated by studying optimization across directions of a number of cost functions. RESULTS: Preferences in both arms to move in the diagonal directions were revealed. The previously suggested tendency to actively accelerate one joint and produce passive motion at the other joint was supported in both arms and load conditions. However, the load increased the tendency to produce strokes in the transverse diagonal directions (perpendicular to the forearm orientation) in both arms. Increases in required muscle effort caused by the load suggested that the higher frequency of movements in the transverse directions represented increased influence of muscle effort minimization on the selection of movement direction. This interpretation was supported by cost function optimization results. CONCLUSIONS: While without load, the contribution of muscle effort minimization was minor, and therefore, not apparent, the load revealed this contribution by enhancing it. Unlike control of interaction torque, the revealed tendency to minimize muscle effort was independent of arm dominance.

Unique features of human movement control predicted by the leading joint hypothesis.

Vaesen suggests that motor control is not among the primary origins of the uniqueness of human tool use. However, recent findings show that cognitive processes involved in control of human limb movements may be much more sophisticated than it was believed previously. The sophistication of movement control may substantially contribute to the uniqueness of humans in tool use.

Interlimb differences of directional biases for stroke production.

Directional preferences during center-out horizontal shoulder-elbow movements were previously characterized for the dominant arm. These preferences were attributed to a tendency to actively accelerate one joint, while exploiting largely passive motion at the other joint. Since the non-dominant arm is known for inefficient coordination of inter-segmental dynamics, here we hypothesized that directional preferences would differ between the arms. A center-out free-stroke drawing task was used that allowed freedom in the selection of movement directions. The task was performed both with and without a secondary cognitive task that has been shown to increase directional biases of the dominant arm. Mirror-symmetrical directional preferences were observed in both arms, with similar bias strength and secondary task effects. The preferred directions were characterized by maximal exploitation of interaction torques for movement production, but only in the dominant arm. The non-dominant arm failed to benefit from interaction torques. The results point to a hierarchical architecture of control. At the higher level, a movement capable to perform the task while satisfying preferences in joint control is specified through forward dynamic transformations. This process is mediated for both arms from a common neural network adapted to the dominant arm and, specifically, to its ability to exploit interaction torques. Dynamic transformations that determine actual control commands are specified at the lower level of control. An alternative interpretation that strokes might be planned evenly across directions, and biases emerge during movement execution due to anisotropic resistance of intrinsic factors that do not depend on arm dominance is also discussed.

The role of vision, speed, and attention in overcoming directional biases during arm movements.

Previous research has revealed directional biases (preferences to select movements in specific directions) during horizontal arm movements with the use of a free-stroke drawing task. The biases were interpreted as a result of a tendency to generate motion at either the shoulder or elbow (leading joint) and move the other (subordinate) joint predominantly passively to avoid neural effort for control of interaction torque. Here, we examined influence of vision, movement speed, and attention on the directional biases. Participants performed the free-stroke drawing task, producing center-out strokes in randomly selected directions. Movements were performed with and without vision and at comfortable and fast pace. A secondary, cognitive task was used to distract attention. Preferred directions remained the same in all conditions. Bias strength mildly increased without vision, especially during fast movements. Striking increases in bias strength were caused by the secondary task, pointing to additional cognitive load associated with selection of movements in the non-preferred directions. Further analyses demonstrated that the tendency to minimize active interference with interaction torque at the subordinate joint matched directional biases in all conditions. This match supports the explanation of directional biases as a result of a tendency to minimize neural effort for interaction torque control. The cognitive load may enhance this tendency in two ways, directly, by reducing neural capacity for interaction torque control, and indirectly, by decreasing capacity of working memory that stores visited directions. The obtained results suggest strong directional biases during daily activities because natural arm movements usually subserve cognitive tasks.

The role of intrinsic factors in control of arm movement direction: implications from directional preferences.

The role of extrinsic and intrinsic factors in control of arm movement direction remains under debate. We addressed this question by investigating preferences in selection of movement direction and whether factors causing these preferences have extrinsic or intrinsic nature. An unconstrained free-stroke drawing task was used during which participants produced straight strokes on a horizontal table, choosing the direction and the beginning and end of each stroke arbitrarily. The variation of the initial arm postures across strokes provided a possibility to distinguish between the extrinsic and intrinsic origins of directional biases. Although participants were encouraged to produce strokes equally in all directions, each participant demonstrated preferences for some directions over the others. However, the preferred directions were not consistent across participants, suggesting no directional preferences in extrinsic space. Consistent biases toward certain directions were revealed in intrinsic space representing initial arm postures. Factors contributing to the revealed preferences were analyzed within the optimal control framework. The major bias was explained by a tendency predicted by the leading joint hypothesis (LJH) to minimize active interference with interaction torque generated by shoulder motion at the elbow. Some minor biases may represent movements of minimal inertial resistance or maximal kinematic manipulability. These results support a crucial role of intrinsic factors in control of the movement direction of the arm. Based on the LJH interpretation of the major bias, we hypothesize that the dominant tendency was to minimize neural effort for control of arm intersegmental dynamics. Possible organization of neural processes underlying optimal selection of movement direction is discussed.

Control of human limb movements: the leading joint hypothesis and its practical applications.

The leading joint hypothesis (LJH) offers a novel interpretation of control of human movements that involve multiple joints. The LJH makes control of each multijoint movement transparent. This review highlights effective applications of the LJH to learning of new motor skills and to analysis of movement changes caused by aging and motor disorders.