Natalia Dounskaia

The internal model and the leading joint hypothesis: implications for control of multi-joint movements

This article presents a theoretical generalization of recent experimental findings accumulated in support of two concepts of inter-segmental dynamics regulation during multi-joint movements. The concepts are the internal model of inter-segmental dynamics and the leading joint hypothesis (LJH). The internal model of limb dynamics is a well-established interpretation of feed-forward control. Recent experiments have generated new information about the organization of the internal model and its role in regulation of inter-segmental dynamics. The LJH, which proposes a simplified principle of the regulation of inter-segmental dynamics, is at the beginning stage of development. This paper outlines major results obtained in these two research directions and demonstrates that the two groups of findings complement and augment each other, suggesting a simple and robust hierarchical strategy of multi-joint movement control that exploits specific mechanical properties of human limbs.

Influence of biomechanical factors on substructure of pointing movements

Irregularities in the velocity profile near the end of pointing movements have been interpreted as corrective submovements whose purpose is to provide accuracy of pointing to the target. The purpose of the present study was to investigate whether two additional factors related to biomechanical properties of the arm also cause submovements. First, motion termination and stabilization of the limb in the final position required by a discrete pointing task may contribute to submovements. Second, inaccurate regulation of interactive torque at the joints may also cause submovements. To investigate the contributions of these two biomechanical factors and the traditionally considered factor of pointing accuracy, the incidence of submovements was analyzed during three types of experimental manipulations. In addition to target size manipulations (small and large targets), conditions for motion termination were manipulated by examining discrete movements (which terminated at the target) and reciprocal movements (which reversed direction without dwelling on the target). Interaction torques were varied by using targets that require different shoulder–elbow coordination patterns. Submovements were detected in 41% of all analyzed movements. Data supported influences from the accuracy and motion termination factors but not from the interactive torque regulation factor on submovement incidence. Gross submovements were associated with motion termination; fine submovements primarily with accuracy demands. These findings and the analysis of temporal movement characteristics suggest that motion termination is an extra movement component that makes control of discrete movements different to control of reciprocal movements. Implications of the findings to a noise-related interpretation of Fitts’ law are discussed. The study emphasizes the influence of arm biomechanics on endpoint kinematics.

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.

Directional interference during bimanual coordination: is interlimb coupling mediated by afferent or efferent processes

The role of afferent information in bimanual directional interference was studied by means of a modulation of the response-produced information in one of both limbs. In Experiment 1, visual information was either present, withdrawn, or shown with a directional transformation on a LCD screen. In Experiment 2, the technique of muscle tendon vibration was used to bias the kinesthetic afferent information associated with movement. The findings revealed strong evidence for directional interference between both limbs. Nevertheless, no evidence could be advanced that the observed interference from the right onto the left limb movement was modulated by manipulation of the afferent sources of information. It is concluded that directional interference primarily emerges at the efferent level of movement planning and organization.

Patterns of Bimanual Interference Reveal Movement Encoding within a Radial Egocentric Reference Frame

Constraints on interlimb coordination have been studied intensively in past years with a primary focus on temporal features. The present study addressed spatial constraints or the degree of directional interference as a function of different line combinations between the upper limbs as well as the modulation of this interference as a result of different board orientations within the performers workspace. This paradigm was used to address a prominent theme in motor neuroscience, namely whether (bimanual) movements are encoded within an allocentric reference frame (pattern of interference invariant with respect to extrinsic space) or within an egocentric reference frame (pattern of interference invariant relative to the center of the performers action space, i.e., intrinsic). The observed patterns of interference revealed that movements are primarily encoded within a radial egocentric reference frame in which the performer is the center of action space. The present psychophysical findings converge with primate single-cell recording studies in which the direction has been identified as a primary movement parameter that is encoded in various brain regions, thereby constituting a principal determinant of bilateral interference.

Origins of submovements during pointing movements

Submovements that are frequently observed in the final portion of pointing movements have traditionally been viewed as pointing accuracy adjustments. Here we re-examine this long-lasting interpretation by developing evidence that many of submovements may be non-corrective fluctuations arising from various sources of motor output variability. In particular, non-corrective submovements may emerge during motion termination and during motion of low speed. The contribution of these factors and the factor of accuracy regulation in submovement production is investigated here by manipulating movement mode (discrete, reciprocal, and passing) and target size (small and large). The three modes provided different temporal combinations of accuracy regulation and motion termination, thus allowing us to disentangle submovements associated with each factor. The target size manipulations further emphasized the role of accuracy regulation and provided variations in movement speed. Gross and fine submovements were distinguished based on the degree of perturbation of smooth motion. It was found that gross submovements were predominantly related to motion termination and not to pointing accuracy regulation. Although fine submovements were more frequent during movements to small than to large targets, other results show that they may also be not corrective submovements but rather motion fluctuations attributed to decreases in movement speed accompanying decreases in target size. Together, the findings challenge the traditional interpretation, suggesting that the majority of submovements are fluctuations emerging from mechanical and neural sources of motion variability. The implications of the findings for the mechanisms responsible for accurate target achievement are discussed.

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.

Biased wrist and finger coordination in Parkinsonian patients during performance of graphical tasks.

Handwriting impairments in Parkinsons disease (PD) have been associated with micrographia, i.e. diminished letter size. However, dyscoordination of the wrist and fingers may also contribute to handwriting deterioration in PD. To investigate this hypothesis, right-handed PD patients and controls were tested in performance of three types of cyclic wrist and finger movements: drawing of two lines and a circle. The line drawing was performed with either simultaneous flexion and extension of the wrist and fingers (equivalent pattern resulting in a right-tilted line) or with wrist flexion/extension accompanied with finger extension/flexion (nonequivalent pattern resulting in a left-tilted line). Circle drawing required a specific phase difference between wrist and finger motions. Movements were performed with an inkless pen on a digitizer-tablet at two frequency levels. Consistent deformations of the circle into right-tilted ovals and lower variability in equivalent compared with nonequivalent lines revealed preference to produce right-tilted shapes. This preference became more apparent with increased movement speed and it was amplified in PD patients. Analysis revealed that the circle deformation emerged mainly due to reduction in relative phase, while wrist and finger amplitudes remained unchanged. The results suggest that PD causes deficit characterized by strong tendency to produce certain coordination patterns between wrist and finger motions. This deficit may significantly contribute to handwriting impairments in PD by reducing the dexterity in the production of the variety of shapes of the cursive letters. Furthermore, the deficiency revealed in wrist and finger coordination may represent a more general deficit affecting control of various multi-joint movements in PD.

The role of different submovement types during pointing to a target

The present study extends our previous findings in challenging the traditional interpretation of irregularities in the velocity profile of pointing movements as corrective submovements performed to improve accuracy of target achievement. The study is driven by a hypothesis that pointing includes at least two subtasks, accurate target achievement and motion termination, each of which can cause submovements (Dounskaia et al. Exp Brain Res 164:505–516, 2005). To investigate submovements associated with these subtasks, two tasks were performed in the experiment. Task 1 was used to examine the contribution of the two subtasks on submovement production by comparing submovements in discrete movements that include motion termination and in cyclic movements during which motion termination is not performed. Target size manipulations emphasized submovements related to the accuracy subtask. The results confirmed that both subtasks included in pointing cause submovements. Gross types of submovements (types 1 and 2) were associated with motion termination and fine submovements (type 3) with accuracy regulation. Task 2 further investigated sources of the accuracy-associated type 3 submovements by including only cyclic movements performed at two levels of frequency. Most (97.6%) of the submovements in task 2 were of type 3. Submovement incidence was strongly (inversely) associated with cyclic frequency, and it was independent of target size. This result questions the accuracy subtask as a primary source for type 3 submovements, and it raises the possibility that these submovements are an inherent property of low-speed movements. Together, results of the two tasks support our previous finding that gross submovements are not necessarily related to accuracy regulation. They also provide evidence that challenges the interpretation of fine submovements as corrections performed voluntarily to improve pointing accuracy. Alternative interpretations of accuracy regulation mechanisms, such as regulation of muscle stiffness and of the muscle co-contraction level are discussed in light of the present results.

Limitations on Coupling of Bimanual Movements Caused by Arm Dominance: When the Muscle Homology Principle Fails

Studies of bimanual movements typically report interference between motions of the two arms and preference to perform mirror-symmetrical patterns. However, recent studies have demonstrated that the two arms differ in the ability to control interaction torque (INT). This predicts limitations in the capability to perform mirror-symmetrical movements. Here, two experiments were performed to test this prediction. The first experiment included bimanual symmetrical and asymmetrical circle drawing at two frequency levels. Unimanual circle drawing was also recorded. The increases in cycling frequency caused differences between the two arms in movement trajectories in both bimanual modes, although the differences were more pronounced in the asymmetrical compared with the symmetrical mode. Based on torque analysis, the differences were attributed to the nondominant arms decreased capability to control INT. The intraarm differences during the symmetrical pattern of bimanual movements were similar (although more pronounced) to those during unimanual movements. This finding was verified in the second experiment for symmetrical bimanual oval drawing. Four oval orientations were used to provide variations in INT. Similar to the first experiment, increases in cycling frequency caused spontaneous deviations from perfect bimanual symmetry associated with inefficient INT control in the nondominant arm. This finding supports the limitations in performing mirror-symmetrical bimanual movements due to differences in joint control between the arms. Based on our results and previous research, we argue that bimanual interference occurs during specification of characteristics of required motion, whereas lower-level generation of muscle forces is independent between the arms. A hierarchical model of bimanual control is proposed.