Filiep Debaere

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.

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.

Brain Areas Involved in Interlimb Coordination: A Distributed Network

Whereas behavioral studies have made significant contributions toward the identification of the principles governing the coordination of limb movements, little is known about the role of higher brain areas that are involved in interlimb coordination. Functional magnetic resonance imaging (fMRI) was used to reveal the brain areas activated during the cyclical coordination of ipsilateral wrist and foot movements. Six normal subjects performed five different tasks that were presented in a random order, i.e., isolated flexion-extension movements of the right wrist (WRIST) and right foot (FOOT), cyclical coordination of wrist and foot according to the isodirectional (ISODIR) and nonisodirectional (NON-ISODIR) mode, and rest (REST). All movements were auditory paced at 66 beats/min. During the coordination of both limb segments, a distributed network was identified showing activation levels in the supplementary motor area (SMA), cingulate motor cortex (CMC), premotor cortex (PMC), primary sensorimotor cortex (M1/S1), and cerebellum that exceeded the sum of the activations observed during the isolated limb movements. In addition, coordination of the limb movements in different directions was associated with extra activation of the SMA as compared to movements in the same direction. It is therefore concluded that the SMA is substantially involved in the coordination of the nonhomologous limbs as part of a distributed motor network. Accordingly, the long-standing exclusive association that has been made between this medial frontal area and bimanual (homologous) coordination needs to be abandoned and extended towards other forms of interlimb coordination (nonhomologous).

Changes in brain activation during the acquisition of a new bimanual coordination task

Motor skill acquisition is associated with the development of automaticity and induces neuroplastic changes in the brain. Using functional magnetic resonance imaging (fMRI), the present study traced learning-related activation changes during the acquisition of a new complex bimanual skill, requiring a difficult spatio-temporal relationship between the limbs, i.e., cyclical flexion-extension movements of both hands with a phase offset of 90 degrees. Subjects were scanned during initial learning and after the coordination pattern was established. Kinematics of the movements were accurately registered and showed that the new skill was acquired well. Learning-related decreases in activation were found in right dorsolateral prefrontal cortex (DLPFC), right premotor, bilateral superior parietal cortex, and left cerebellar lobule VI. Conversely, learning-related increases in activation were observed in bilateral primary motor cortex, bilateral superior temporal gyrus, bilateral cingulate motor cortex (CMC), left premotor cortex, cerebellar dentate nuclei/lobule III/IV/Crus I, putamen/globus pallidus and thalamus. Accordingly, bimanual skill learning was associated with a shift in activation among cortico-subcortical regions, providing further evidence for the existence of differential cortico-subcortical circuits preferentially involved during the early and advanced stages of learning. The observed activation changes account for the transition from highly attention-demanding task performance, involving processing of sensory information and corrective action planning, to automatic performance based on memory representations and forward control.

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.

Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency.

In the present functional magnetic resonance imaging (fMRI) study, we assessed the neural network governing bimanual coordination during manipulations of spatiotemporal complexity and cycling frequency. A parametric analysis was applied to determine the effects of each of both factors as well as their interaction. Subjects performed four different cyclical movement tasks of increasing spatiotemporal complexity (i.e., unimanual left-right hand movements, bimanual in-phase movements, bimanual anti-phase movements, and bimanual 90 degrees out-of-phase movements) across four frequency levels (0.9, 1.2, 1.5, and 1.8 Hz). Results showed that, within the network involved in bimanual coordination, functional subcircuits could be distinguished: Activation in the supplementary motor area, superior parietal cortex (SPS), and thalamic VPL Nc was mainly correlated with increasing spatiotemporal complexity of the limb movements, suggesting that these areas are involved in higher-order movement control. By contrast, activation within the primary motor cortex, cingulate motor cortex (CMC), globus pallidus, and thalamic VLo Nc correlated mainly with movement frequency, indicating that these areas play an important role during movement execution. Interestingly, the cerebellum and the dorsal premotor cortex were identified as the principal regions responding to manipulation of both parameters and exhibiting clear interaction effects. Therefore, it is concluded that both areas represent critical sites for the control of bimanual coordination.

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.

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. Hum Brain Mapp, 2005.

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 Parkinsons 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.

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

Abstract. 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.