Grasping an object requires processing visuospatial information about the extrinsic features (spatial location) and intrinsic features (size, shape, orientation) of the object. Accordingly, manual prehension has been subdivided into a reach component, guiding the hand toward the object on the basis of its extrinsic features, and a grasp component, preshaping the fingers around the center of mass of the object on the basis of its intrinsic features. In neural terms, this distinction has been linked to a dedicated dorsomedial "reaching" circuit and a dorsolateral "grasping" circuit that process extrinsic and intrinsic features, linking occipital areas via parietal regions with the dorsal and ventral premotor cortex, respectively. We have tested an alternative possibility, namely that the relative contribution of the two circuits is related to the degree of on-line control required by the prehension movement.We used dynamic causal modeling of functional magnetic resonance imaging time series to assess how parieto-frontal connectivity is modulated by planning and executing prehension movements toward objects of different size and width. This experimental manipulation evoked different movements, with different planning and execution phases for the different objects. Crucially, grasping large objects increased inter-regional couplings within the dorsomedial circuit, whereas grasping small objects increased the effective connectivity of a mainly dorsolateral circuit, with a degree of overlap between these circuits. These results argue against the presence of dedicated cerebral circuits for reaching and grasping, suggesting that the contributions of the dorsolateral and the dorsomedial circuits are a function of the degree of on-line control required by the movement.
Adaptive behavior requires an organism to evaluate the outcome of its actions, such that future behavior can be adjusted accordingly and the appropriate response selected. During associative learning, the time at which such evaluative information is available changes as learning progresses, from the delivery of performance feedback early in learning to the execution of the response itself during learned performance. Here, we report a learning-dependent shift in the timing of activation in the rostral cingulate zone of the anterior cingulate cortex from external error feedback to internal error detection. This pattern of activity is seen only in the anterior cingulate, not in the presupplementary motor area. The dynamics of these reciprocal changes are consistent with the claim that the rostral cingulate zone is involved in response selection on the basis of the expected outcome of an action. Specifically, these data illustrate how the anterior cingulate receives evaluative information, indicating that an action has not produced the desired result. D
The posterior parietal cortex (PPC) is known to be involved in the control of automatic movements that are spatially guided, such as grasping an apple. We considered whether the PPC might also contribute to the performance of visuomotor associations in which stimuli and responses are linked arbitrarily, such as producing a certain sound for a typographical character when reading aloud or pressing pedals according to the color of a traffic light when driving a motor vehicle. The PPC does not appear to be necessary for learning new arbitrary visuomotor associations, but with extensive training, the PPC can encode nonspatial sensory features of task-relevant cues. Accordingly, we have tested whether the contributions of the PPC might become apparent once arbitrary sensorimotor mappings are overlearned.We have used functional magnetic resonance imaging to measure cerebral activity while subjects were learning novel arbitrary visuomotor associations, overlearning known mappings, or attempting to learn frequently changing novel mappings. To capture the dynamic features of cerebral activity related to the learning process, we have compared time-varying modulations of activity between conditions rather than average (steady-state) responses.Frontal, striatal, and intraparietal regions showed decreasing or stable activity when subjects learned or attempted to learn novel associations, respectively. Importantly, the same frontal, striatal, and intraparietal regions showed time-dependent increases in activity over time as the mappings become overlearned, i.e., despite time-invariant behavioral responses. The automaticity of these mappings predicted the degree of intraparietal changes, indicating that the contribution of the PPC might be related to a particular stage of the overlearning process. We suggest that, as the visuomotor mappings become robust to interference, the PPC may convey relevant sensory information toward the motor cortex. More generally, our findings illustrate how rich cerebral dynamics can underlie stable behavior.
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