Neural control of on-line guidance of hand reaching movements

Abstract

Orienting one's gaze towards a peripheral target is usually composed of a hypometric primary saccade followed by a secondary 'corrective saccade' triggered automatically (without conscious perception) by the retinal error at the end of the primary saccade and characterised by a short latency. Due to visual suppression during the saccade, the artificial introduction of a random small target jump during that short period remains undetected and triggers after the end of the primary saccade a normal 'corrective saccade'. As a result this procedure simulates an error in the planning of the primary saccade. On the other hand optimum hand pointing (trade-off between movement time and accuracy) is considered classically to involve a natural parallel initiation of saccade and hand response based on a poor peripheral retinal location, and a further amendment of the hand motor response based on the retinal error provided by the simultaneous vision of target and hand during the movement home phase. To test the hypothesis that the retinal feedback at the end of the primary saccade is used to update the visual target position and amend the ongoing hand motor response, we developed a paradigm involving both an optimum hand pointing and an undetected random target perturbation during the orienting saccade. In order to show that the amendments were controlled by a loop comparing the perceived target location with the dynamic hand position signal, vision of the limb was removed at movement onset. Results showed that the movement was smoothly monitored on-line without additional time processing demands. This functional property of flexibility of the ongoing hand motor response, was generalized from movement extent to movement direction. The undetectability of the perturbation at a conscious level was not a prerequisite for motor flexibility, which was further shown to depend on a critical phase of the limb movement beyond which the latter was no longer amendable, even when the limb was visible. The hand pointing flexibility was further generalised from pointing to the more complex hand reaching and grasping process. It was shown that the flexibility of both the transport and the grasp components were closely coupled. A careful analysis of the data suggested the controlled variable to be the general posture of the upper limb, reaching Bernstein's intuitions about redundancy reduction in skeletomotor systems with degrees of freedom in excess. A kinematics study of the motor flexibility of reaching and grasping in a patient with a bilateral optic ataxia favoured the idea of a posterior parietal cortex involvement in the error processing underlying motor flexibility, reaching the same conclusions as other recent studies using either Positron Emission Tomography or Transcranial Magnetic Stimulation.