Information processing in human parieto-frontal circuits during goal-directed bimanual movements.

It is known that, in macaques, movements guided by somatosensory information engage anterior parietal and posterior precentral regions. Movements performed with both visual and somatosensory feedback additionally activate posterior parietal and anterior precentral areas. It remains unclear whether the human parieto-frontal circuits exhibit a similar functional organization. Here, we employed a directional interference task requiring a continuous update of sensory information for the on-line control of movement direction, while brain activity was measured by functional magnetic resonance imaging (fMRI). Directional interference arises when bimanual movements occur along different directions in joint space. Under these circumstances, the presence of visual information does not substantially alter performance, such that we could vary the amount and type of sensory information used during on-line guidance of goal-directed movements without affecting motor output. Our results confirmed that in humans, as in macaques, movements guided by somatosensory information engages anterior parietal and posterior precentral regions, while movements performed with both visual and somatosensory information activate posterior parietal and anterior precentral areas. We provide novel evidence on how the interaction of specific portions of the dorsal parietal and precentral cortex in the right hemisphere might generate spatial representations by integrating different sensory modalities during goal-directed movements.

The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour.

Behavioral studies in humans have shown that bimanual coordination imposes specific demands on the central nervous system that exceed unimanual task control. In the present study we used functional magnetic resonance imaging to investigate the neural correlate of this additional coordination effort, i.e. regions responding more strongly to bimanual movements than inferred from summing up the responses to the unimanual subtasks. Subjects were scanned while performing movements along different directions, either uni- or bimanually. During the bimanual condition, trajectories of movement of the left and right hand were spatially incompatible, such that additional effort was required to break away from intrinsically favored mirror-movements and to integrate movements of both limbs into a new spatial pattern. Our main finding was that the execution of spatially complex bimanual coordination as compared with the unimanual subtasks activated the anterior cingulate cortex (posterior part) as well as the dorso-anterior precuneus. We hypothesize that the anterior cingulate exerts its modulatory effect on other motor areas, such as the primary motor cortex and the supplementary motor area, in order to suppress intrinsically favored coordination tendencies. Conversely, the precuneus is likely to be involved in shifting attention between different locations in space, which was necessary for monitoring the trajectories of the left and right wrist when both limbs moved in parallel. Our findings suggest that the coordination effort during bimanual and perhaps other modes of coordinated behavior is mediated by regions contributing to higher order functions, which form an interface between cognition and action.

Neural basis of aging: the penetration of cognition into action control.

Although functional imaging studies have frequently examined age-related changes in neural recruitment during cognitive tasks, much less is known about such changes during motor performance. In the present study, we used functional magnetic resonance imaging to investigate age-related changes in cyclical hand and/or foot movements across different degrees of complexity. Right-handed volunteers (11 young, 10 old) were scanned while performing isolated flexion-extension movements of the right wrist and foot as well as their coordination, according to the "easy" isodirectional and "difficult" nonisodirectional mode. Findings revealed activation of a typical motor network in both age groups, but several additional brain areas were involved in the elderly. Regardless of the performed motor task, the elderly exhibited additional activation in areas involved in sensory processing and integration, such as contralateral anterior insula, frontal operculum, superior temporal gyrus, supramarginal gyrus, secondary somatosensory area, and ipsilateral precuneus. Age-related activation differences during coordination of both segments were additionally observed in areas reflecting increased cognitive monitoring of motor performance, such as the pre-supplementary motor area, pre-dorsal premotor area, rostral cingulate, and prefrontal cortex. In the most complex coordination task, the elderly exhibited additional activation in anterior rostral cingulate and dorsolateral prefrontal cortex, known to be involved in suppression of prepotent response tendencies and inhibitory cognitive control. Overall, these findings are indicative of an age-related shift along the continuum from automatic to more controlled processing of movement. This increased cognitive monitoring of movement refers to enhanced attentional deployment, more pronounced processing of sensory information, and intersensory integration.

Spatial interference during bimanual coordination: differential brain networks associated with control of movement amplitude and direction.

Bimanual interference emerges when spatial features, such as movement direction or amplitude, differ between limbs, as indicated by a mutual bias of limb trajectories. Although first insights into the neural basis of directional interference have been revealed recently, little is known about the neural network associated with amplitude interference. We investigated whether amplitude versus directional interference activates differential networks. Functional magnetic resonance imaging (fMRI) was applied while subjects performed cyclical, bimanual joystick movements with either the same vs. different amplitudes, directions, or both. The kinematic analysis confirmed that subjects experienced amplitude interference when they moved with different as compared to the same amplitude, and directional interference when they moved along different as compared to the same direction. On the brain level, amplitude and directional interference both resulted in activation of a bilateral superior parietal-premotor network, which is known to contribute to sensorimotor transformations during goal-directed movements. Interestingly, amplitude but not directional interference exclusively activated a bilateral network containing the dorsolateral prefrontal cortex, anterior cingulate, and supramarginal gyrus, which was shown previously to contribute to executive functions. Even though the encoding of amplitude and directional information converged and activated the same neural substrate, our data thus show that additional and partly independent mechanisms are involved in bimanual amplitude as compared to that in directional control.

Ipsilateral coordination deficits and central processing requirements associated with coordination as a function of aging.

Young and elderly participants performed concurrent ipsilateral hand-foot movements either isodirectionally or nonisodirectionally. We determined performance by measuring the maximal cycling frequency at which the coordination pattern could be performed successfully (CF(max)). We also determined attentional costs by means of a dual-task paradigm. Findings revealed that CF(max) was significantly lower in the elderly than in the young participants for the nonisodirectional mode, whereas we observed no differences for the isodirectional mode. Under dual-task conditions, coordination deteriorated in the elderly group only. However, when we equated levels of task difficulty, differences between the groups disappeared. Furthermore, attentional costs did not differ between isodirectional and nonisodirectional movements. This indicates that age-related coordination deficits were not primarily evoked by reduced attentional resources or control in elderly persons.

Parieto-premotor areas mediate directional interference during bimanual movements.

In bimanual movements, interference emerges when limbs are moved simultaneously along incompatible directions. The neural substrate and mechanisms underlying this phenomenon are largely unknown. We used functional magnetic resonance imaging to compare brain activation during directional incompatible versus compatible bimanual movements. Our main results were that directional interference emerges primarily within superior parietal, intraparietal and dorsal premotor areas of the right hemisphere. The same areas were also activated when the unimanual subtasks were executed in isolation. In light of previous findings in monkeys and humans, we conclude that directional interference activates a parieto-premotor circuit that is involved in the control of goal-directed movements under somatosensory guidance. Moreover, our data suggest that the parietal cortex might represent an important locus for integrating spatial aspects of the limbs' movements into a common action. It is hypothesized to be the candidate structure from where interference arises when directionally incompatible movements are performed. We discuss the possibility that interference emerges when computational resources in these parietal areas are insufficient to code two incompatible movement directions independently from each other.

Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback.

It is commonly agreed that a functional dissociation with respect to the internal vs external control of movements exists for several brain regions. This has, however, only been tested in relation to the timing and preparation of motor responses, but not to ongoing movement control. Using functional magnetic resonance imaging (fMRI), the present study addressed the neuroanatomical substrate of the internal-external control hypothesis by comparing regional brain activation for cyclical bimanual movements performed in the presence or absence of augmented visual feedback. Subjects performed a bimanual movement pattern, either with the help of on-line visual feedback of the movements (externally guided coordination) or with the eyes closed on the basis of an internal representation of the movement pattern (internally generated coordination). Visual control and baseline rest conditions were also added. Results showed a clear functional dissociation within the network involved in movement coordination. The hMT/V5+, the superior parietal cortex, the premotor cortex, the thalamus, and cerebellar lobule VI showed higher activation levels when movements were guided by visual feedback. Conversely, the basal ganglia, the supplementary motor area, cingulate motor cortex, the inferior parietal, frontal operculum, and cerebellar lobule IV-V/dentate nucleus showed higher involvement when movements were internally generated. Consequently, the present findings suggest the existence of distinct cortico-cortical and subcortico-cortical neural pathways for externally (augmented feedback) and internally guided cyclical bimanual movements. This provides a neurophysiological account for the beneficial effect of providing augmented visual feedback to optimize movements in normal and motor disordered patients.