Understanding bimanual coordination across small time scales from an electrophysiological perspective.

Bimanual movement involves a variety of coordinated functions, ranging from elementary patterns that are performed automatically to complex patterns that require practice to be performed skillfully. The neural dynamics accompanying these coordination patterns are complex and rapid. By means of electro- and magneto-encephalographic approaches, it has been possible to examine these dynamics during bimanual coordination with excellent temporal resolution, which complements other neuroimaging modalities with superb spatial resolution. This review focuses on EEG/MEG studies that unravel the processes involved in movement planning and execution, motor learning, and executive functions involved in task switching and dual tasking. Evidence is presented for a spatio-temporal reorganization of the neural networks within and between hemispheres to meet increased task difficulty demands, induced or spontaneous switches in coordination mode, or training-induced neuroplastic modulation in coordination dynamics. Future theoretical developments will benefit from the integration of research techniques unraveling neural activity at different time scales. Ultimately this work will contribute to a better understanding of how the human brain orchestrates complex behavior via the implementation of inter- and intra-hemispheric coordination networks.

Primary motor cortex and ipsilateral control: a TMS study.

In this transcranial magnetic stimulation study, we assessed motor cortex excitability in the resting hemisphere while the homologous side was active during a voluntary unimanual task. Data acquired from left- and right-handers showed that cortical excitability varied as a function of isometric task demands and hand dominance. In particular, facilitation of the motor-evoked potentials was observed across task requirements in left-handers, independent of which hemisphere was active. In right-handers, facilitation was present when the right hemisphere was active whereas this effect was largely reduced when the left hemisphere was active, suggesting pronounced inhibitory interactions from the left (dominant) to the right (non-dominant) hemisphere. The distinct scaling of motor cortex excitability indicates the importance of the left hemisphere in guiding manual control in right-handers whereas both hemispheres are functionally relevant in left-handers. Overall, the results underline the asymmetrical organization of the motor system in right-handers with an important role of the dominant hemisphere whereas symmetrical functional abilities of both hemispheres characterize left-handers.

Neurological problems affecting hand dexterity.

The first objective of this review is to summarize how grip force and load force (holding and transporting forces) are coordinated. Usually, the two forces vary in parallel, thereby resulting in a constant force ratio. Departures from this rule have been observed, however, depending on dynamic task constraints. The second objective is to summarize some of the pathophysiology of grasping in movement disorders. By means of a drawer-pulling task, regulation of grip force was analyzed when pulling was perturbed either by self-induced or externally applied load disturbances. Normal subjects automatically increased grip force in anticipation to the expected load. In the same situation, hemiparetic patients failed to generate proactive grip force and frequent slips were observed. Cerebellar patients were shown to adopt a 'default' strategy in producing high grip force output when the drawer had to be pulled up to its mechanical stop. This differed from the more flexible normal mode of raising grip force in accord with the pulling speed. In patients with Huntington's Chorea, grip/load force coordination differed from that of normal subjects, as expressed in an overscaled grip force. This might be a secondary, less flexible 'default' strategy to overcome the failure in adapting grip force to upcoming disturbances. Writer's cramp patients overscaled grip force in both the dominant and non-dominant hand, and grip force further increased when hand muscles were vibrated, suggesting an abnormal sensorimotor integration. The results illustrate the degrading consequences of cortical and subcortical pathology on manual dexterity, which is sometimes partly compensated for by new, less flexible default strategies.

Proprioceptive regulation of interlimb behavior: interference between passive movement and active coordination dynamics.

The coordination of homolateral effectors (right arm/right leg) according to the in-phase or anti-phase mode was perturbed through passive movement of a third segment (left arm or left leg) imposed by the experimenter. The manipulated parameters of the passive segment were frequency and amplitude along with their degree of scaling. Results showed that passive movement degraded anti-phase patterns more than in-phase patterns. Furthermore, the anti-phase mode deteriorated profoundly during frequency manipulation, but scaling did not induce additional effects, whereas a linear association was observed between anti-phase deterioration and amplitude manipulation. Together, these data indicate that passive movement disturbed the coordination dynamics of an actively performed task. The fact that interference depended on the manipulated parameter suggests a distinction in the degree of intrusiveness of the irrelevant afferent information induced by the passive limb. It is concluded that sensory discrimination between irrelevant and relevant input is critical in performing a coordinated task adequately under perturbed conditions.

Regulation of grasping forces during bimanual in-phase and anti-phase coordination.

When a hand-held object is moved, grip force is adapted in an anticipatory manner to load force due to a dynamic coupling between both forces. The present study addressed the issue of grip-load force regulation when moving rhythmically two hand-held objects in the vertical dimension, and more specifically the divergence of force control when performing according to the in-phase versus anti-phase mode. Results revealed that grip-load force ratio profiles were similar in both bimanual conditions. That is, force ratio was not constant throughout the movement cycles but followed a fairly regular pattern with maxima and minima, attained at upward and downward hand positions, respectively. However, anti-phase patterns showed an increased maximum grip-load force ratio as compared to in-phase patterns, whereas the latter did not differ from unimanual movements. The magnification of maximum force ratio during anti-phase movements suggests that rescaling occurred. This is likely due to the complexity of the anti-phase mode that necessitates increased monitoring and attention relative to the other performance conditions, creating a coordinative situation that imposes an additional degree of uncertainty. Therefore, the safety margin is amplified during anti-phase movements, probably as a strategy to prevent a potential destabilization of the grip during an asymmetrical load condition. Accordingly, these findings also demonstrate that grip-load force regulation is more proficiently controlled during bimanual in-phase than anti-phase movements. Herewith, the data add content to earlier work illustrating kinematic dissimilarities between both coordination modes.

Toward a physiological understanding of human dexterity.

Dexterity, defined as the skillful manipulation of the hands, is now amenable to physiological investigation. Two topics are discussed here: grasping (i.e., hand-object coupling) and bimanual coordination. Dexterity depends on powerful, distributed neural networks and is particularly vulnerable to brain lesions. A knowledge of physiological mechanisms is needed to deal with these neurological problems.

Damage to the parietal lobe impairs bimanual coordination.

Moving the upper limbs at a common tempo according to a mirror or parallel mode represents elementary coordination dynamics. Previously, the role of the medial wall areas have been emphasized for successful production of these bimanual patterns. The involvement of the parietal lobe is less clear despite its importance for the representation of motor skill and sensorimotor integration. The objective of this study was to investigate temporal control in patients with parietal pathology when performing isofrequency configurations. As compared to control subjects, these patients showed desynchronization of movement trajectories that was most apparent during parallel patterns. These observations suggest the significant role of the parietal lobe for bimanual coordination which becomes increasingly relevant as a function of task complexity.

Bimanual organization of manipulative forces: evidence from erroneous feedforward programming of precision grip.

The objective of the present study was to investigate grip-load force regulation during a bimanual lifting task with two hand-held objects. Various conditions were included during which the weight of one or both objects was changed in an unpredictable order every fourth trial. Results showed that force control of heavy weight movements preceded by light weight movements was not strongly influenced across trials. Conversely, force responses of light weight movements preceded by heavy weight movements were overestimated due to an augmented degree of grip force. However, successful updating of force output occurred after one trial. Furthermore, bimanual interactions between the grasping forces were observed, suggestive of a coordinative command that assimilated the individual response specifications. The latter also became apparent from a similar grip-load force ratio for both hands when the objects' physical properties had become predictable, independent of the forces that were produced according to the individual weight requirements. These data indicate that the grip-load force ratio is the controlled variable for bimanual manipulative behaviour.

Grip force scaling and sequencing of events during a manipulative task in Huntington's disease.

The aim of the study was to investigate force regulation and sequencing of events in Huntington's disease (HD) patients when performing a drawer opening task using the precision grip. Results revealed that HD patients used excessive grip force levels that were unrelated to the actual task demands. Also, they demonstrated a higher grip force value at load force onset in addition to an increased delay between initiation of grip force and load (pulling) force. These data indicate a deficit in the coordinated activation of both forces due to HD. Furthermore, the patients showed bradykinesia along with a prolonged interval between the movement phases underlying the task, denoting an impairment in encoding serially ordered events. Together, these results illustrate the deteriorating effect of striatal pathology on manual function. Accordingly, an amended control of grasping forces and serial encoding of movement-related events due to HD are likely to affect the proficiency of common manipulative skills.

Dissociation of grip/load-force coupling during a bimanual manipulative assignment.

The aim of the present study was to examine interlimb interactions of grasping forces during a bimanual manipulative assignment that required the execution of a drawer-opening task with the left hand and an object-holding task with the right hand. Compared with the unimanual performance, the grip/load-force ratio of the object-holding task was shifted towards that of the simultaneously executed drawer-opening task. This shows that force parameterization of the dynamic activity interacted with that of the static activity. That the increased force ratio only involved modification of grip force, while load force was held constant, indicates a disruption of the commonly observed co-variation of both forces during a manipulative action. These data are consistent with the notion that the coordinative constraint between grip and load force is a flexible parameter.

A higher-order mechanism overrules the automatic grip-load force constraint during bimanual asymmetrical movements.

The aim of the present study was to examine grip-load force regulation during unimanual and bimanual movements. Two protocols were included which manipulated the object's weight and covered distance. Results showed that grip-load ratio was adapted to the task requirements. During unimanual and bimanual symmetrical movements, an increased grip-load force ratio for long versus short amplitude movements as well as for light versus heavy weight movements was noted. These findings could be related to the observed movement speed variations associated with the tasks. During bimanual asymmetrical movements, the grip-load force ratio became comparable for both sides. When transporting different object's weights to constant distances, the grip-load force ratio of light weight movements decreased towards that of heavy weight movements. As movement speed was reduced, it indicates that grasping forces were adapted accordingly. When transporting constant object's weights to different distances, the grip-load force ratio of short amplitude movements increased towards that of long amplitude movements. Since movement speed was decreased, it suggests that a bimanual coordinative command overruled the automatic grip-load coupling. In conclusion, these data show that interlimb coupling induced a rescaling towards a common control structure, leading to similar grasping forces during bimanual movements with dissimilar actions.

Role of the corpus callosum in bimanual coordination: a comparison of patients with congenital and acquired callosal damage.

The objective of the study was to investigate temporal control in patients with congenital as compared to acquired pathology of the corpus callosum during two different bimanual paradigms: (i) a drawer-opening task during which one hand opened a drawer while the other hand reached and grasped a small object, and (ii) rhythmical circling movements that were executed according to the in-phase or antiphase mode. Synchronization values revealed that patients with acquired callosal dysfunction generally showed optimal behaviour during the goal-directed and familiar drawer-opening task but demonstrated strong tendencies towards desynchronization during circling movements, which became most apparent for antiphase coordination. Whereas one patient with callosal agenesis showed a similar performance, the other acallosal patients performed both activities successfully. These observations indicate that patients with congenital absence of the corpus callosum can make use of compensatory mechanisms for allowing temporal synchronization during bimanual movements whereas patients with acquired callosal dysfunction are severely hampered when the task places significant demands on the control processes. The data also underline that the ability of callosal patients to precisely time events in coordinated actions depend on the task constraints.

Bimanual coordination and limb-specific parameterization in patients with Parkinson's disease.

Bimanual coordination and the capability to parameterize the individual limb movements were examined in patients with Parkinson's disease (PD) as compared to healthy control subjects. In-phase and anti-phase patterns were performed while the individual limb movements were subjected to amplitude and loading manipulations. Findings showed that PD patients produced the bimanual configurations with lower degrees of phasing accuracy and consistency than control subjects, indicating an impairment at the global (coordinative) level of simultaneously produced movements. At the local (limb-specific) level, the imposed distances with and without loading were unaffected in PD patients as compared to control subjects, whereas cycle times were prolonged and depended on the task requirements. This illustrates a disturbance at the limb-specific level in complying with the execution of the submovements. The finding that movement slowness only became evident in the more complex conditions, suggests that it did not mainly represent a deficit in the execution of coordinated movements, but rather an inability to accommodate the motor output during stringent spatiotemporal task constraints.

Age-related deterioration of coordinated interlimb behavior.

Younger and older participants performed two-limb coordination patterns of homologous (similar) and nonhomologous (dissimilar) effectors during 1:1 synchronization, according to the in-phase or anti-phase mode. The aim of the study was to examine age-related changes during the production of these basic movement patterns and their relative stability difference. The findings revealed that the aging process modulated the coordination dynamics as a function of effector system characteristics. Whereas the homologous system was resistant to age-related deficits, movements of the nonhomologous system showed coordinative degradation that was most apparent during execution of the anti-phase mode. The latter performance regression is argued to be an expression of age-dependent declines in cognitive regulation and afferent information processing. This implies that deterioration in coordinated behavior across the life span may be strongly task dependent because of a combined effect of cognitive and sensory components.

Disturbed sensorimotor processing during control of precision grip in patients with writer's cramp.

The aim of the study was to investigate force regulation in patients with writer's cramp when performing a drawer-opening task using the precision grip. Experimental conditions included intervening load pulses and vibratory manipulations for examining grip force responses to sensory disturbances. The data revealed that grip force was increased in patients with writer's cramp compared with normal subjects, with a stronger modulation in the symptomatic compared with the asymptomatic hand. This denotes a change in force scaling capabilities and most notably for the preferred hand used in manipulative activities. Vibratory stimulation of the extrinsic hand/finger muscles resulted in an increased grip force of both hands in the patients with writer's cramp. The latter was not observed in normal subjects and supports a bilateral dysfunction in sensorimotor integration resulting from focal dystonia. In conclusion, the disturbed regulation of the precision grip during a drawer-opening task is illustrative for the inability of patients with writer's cramp to efficiently control the force output during manipulative activities.

Temporal control of a bimanual task in patients with cerebellar dysfunction.

The objective of the study was to investigate whether temporal control during a goal-directed bimanual action is disturbed in cerebellar patients. The task was to open a drawer with one hand and to reach and grasp a small object with the other hand. Interlimb coupling was determined at start and end positions. Cerebellar patients as compared to normal subjects showed an increased offset for initiating the hand movements which denotes the involvement of the cerebellum for organizing the components underlying the bimanual task. The reduced simultaneity was caused by a delayed movement onset of the grasping (non-leading) hand as compared to the pulling hand. Lack of vision increased the degree of desynchronization for the patients at the start position, indicating that they depended on external cues for organizing the temporal coordinates of the combined motion pattern. At the goal, the magnitude of temporal offset was similar/smaller than at movement onset which can be related to feedforward mechanisms that are used to anticipate the limbs' end positions. These results confirm the role of the cerebellum for planning the temporal ordering of movement sequences into a synergic action.

Role of the cerebellum in tuning anticipatory and reactive grip force responses.

The aim of our study was to determine if load perturbations that could destabilize grasp control are adequately controlled by cerebellar patients. We examined patients with unilateral cerebellar lesions who had largely recovered from their initial symptoms and compared grip force regulation for the affected and unaffected hand during a drawer-opening task. Two experimental paradigms were included: (1) a brief load perturbation during a self-stopped drawer pull and (2) a loading impact when the drawer was pulled out to the mechanical stop. The results showed that when a self-stopped movement was perturbed during its trajectory, anticipatory grip force increase was smaller for the affected than for the unaffected hand, illustrating a disturbed gain control due to cerebellar dysfunction. When the mechanical stop arrested the movement, the amount of grip force did not differ significantly between the affected and unaffected side; however, both hands used different control strategies. Whereas the unaffected hand anticipated the load perturbation by a ramp-like increase of grip force toward the impending impact, the affected hand increased grip force at movement onset to a default level and maintained this value until the task was ended. In addition, the latency between impact and reactive peak in grip force was prolonged for the affected hand, suggesting a delayed cerebellar transmission of reactive responses. In conclusion, these findings demonstrate that the cerebellum is involved in anticipatory and reactive mechanisms dealing with load perturbations during goal-directed behavior.

Intentional switching between behavioral patterns of homologous and nonhomologous effector combinations.

Intentional switching between preferred coordination modes (Experiment 1) and between isofrequency and multifrequency conditions (Experiments 2 and 3) was compared across different effector combinations. Experiment 1 showed that homologous limbs switched faster toward the in-phase and anti-phase mode than nonhomologous limbs, supporting their distinct degree of coordinative stability during 1:1 synchronization. Experiments 2 and 3 revealed that switching time between isofrequency and multifrequency conditions depended on the attractiveness of both coordination dynamics associated with the combination of segments involved. These results are consistent with the unique prediction derived from dynamic pattern approach in which the differential stability of the coordination modes determines the switching time.

Grip-load force coordination in cerebellar patients.

The study examined the anticipatory grip force modulations to load force changes during a drawer-opening task. An impact force was induced by a mechanical stop which abruptly arrested movement of the pulling hand. In performing this task, normal subjects generated a typical grip force profile characterized by an initial force impulse related to drawer movement onset, followed by a ramp-like grip force increase prior to the impending load perturbation. Finally, a reactive response was triggered by the impact. In patients with bilateral cerebellar dysfunction, the drawer-opening task was performed with an alternative control strategy. During pulling, grip force was increased to a high (overestimated) default level. The latter suggests that cerebellar patients were unable to adjust and to scale precisely the grip force according to the load force. In addition, the latency between impact and reactive activity was prolonged in the patients, suggesting an impaired cerebellar transmission of the long-latency responses. In conclusion, these data demonstrate the involvement of cerebellar circuits in both proactive and reactive mechanisms in view of predictable load perturbations during manipulative behavior.

The identification of coordination constraints across planes of motion.

Two dominant coordination constraints have been identified during isofrequency conditions in previous work: the egocentric constraint, i.e., simultaneous activation of homologous muscle groups, and the allocentric constraint, i.e., moving the segments in the same direction in extrinsic space. To verify their generalization, bimanual drawing movements were performed in different planes of motion (transverse, frontal, sagittal, frontal-transverse) according to the in-phase and anti-phase mode along the X- and Y-axes. Convergent findings were obtained across the transverse, frontal, and frontal-transverse planes. The in-phase mode along both axes was performed most accurately/consistently, whereas the anti-phase mode resulted in a deterioration of the coordination pattern and this effect was most pronounced when the latter mode was introduced with respect to both dimensions. For sagittal plane motions, the in-phase mode was again superior but the second most optimal configuration was the anti-phase mode along both axes. This finding was hypothesized to result from the familiarity with the pattern since it resembles cycling behavior. It illustrates how cognitive mapping is superimposed onto the dynamics of interlimb coordination. Overall, these results support the presence of both the egocentric and allocentric constraint during bimanual movement production.