Michel Desmurget

Forward modeling allows feedback control for fast reaching movements

Delays in sensorimotor loops have led to the proposal that reaching movements are primarily under pre-programmed control and that sensory feedback loops exert an influence only at the very end of a trajectory. The present review challenges this view. Although behavioral data suggest that a motor plan is assembled prior to the onset of movement, more recent studies have indicated that this initial plan does not unfold unaltered, but is updated continuously by internal feedback loops. These loops rely on a forward model that integrates the sensory inflow and motor outflow to evaluate the consequence of the motor commands sent to a limb, such as the arm. In such a model, the probable position and velocity of an effector can be estimated with negligible delays and even predicted in advance, thus making feedback strategies possible for fast reaching movements. The parietal lobe and cerebellum appear to play a crucial role in this process. The ability of the motor system to estimate the future state of the limb might be an evolutionary substrate for mental operations that require an estimate of sequelae in the immediate future.

Role of the posterior parietal cortex in updating reaching movements to a visual target

The exact role of posterior parietal cortex (PPC) in visually directed reaching is unknown. We propose that, by building an internal representation of instantaneous hand location, PPC computes a dynamic motor error used by motor centers to correct the ongoing trajectory. With unseen right hands, five subjects pointed to visual targets that either remained stationary or moved during saccadic eye movements. Transcranial magnetic stimulation (TMS) was applied over the left PPC during target presentation. Stimulation disrupted path corrections that normally occur in response to target jumps, but had no effect on those directed at stationary targets. Furthermore, left-hand movement corrections were not blocked, ruling out visual or oculomotor effects of stimulation.

An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia

We designed a protocol distinguishing between automatic and intentional motor reactions to changes in target location triggered at movement onset. In response to target jumps, but not to a similar change cued by a color switch, normal subjects often could not avoid automatically correcting fast aiming movements. This suggests that an ‘automatic pilot’ relying on spatial vision drives fast corrective arm movements that can escape intentional control. In a patient with a bilateral posterior parietal cortex (PPC) lesion, motor corrections could only be slow and deliberate. We propose that ‘on-line’ control is the most specific function of the PPC and that optic ataxia could result from a disruption of automatic hand guidance.

Movement Intention After Parietal Cortex Stimulation in Humans

Consciousness and Intention Where in the brain are our intentions formed and how do we become aware of these intentions? Desmurget et al. (p. 811; see the Perspective by Haggard) investigated the effect of direct cortical stimulation of parietal and premotor regions in patients undergoing brain surgery for tumor removal. Stimulation of the parietal lobe provoked the conscious experience of wanting to move the upper limb, lips, or tongue without any concomitant motor activity. When stimulation intensity was increased, patients believed that they had actually moved or talked, but again no muscle activity was detected. When, however, the premotor region of the frontal lobes was stimulated, real complex multijoint movements were induced. However, patients did not experience these movements as produced by a conscious internal act of will. Indeed, they were not even aware that they had moved. Increasing stimulation intensity increased the amplitude or complexity of the movement but never made it reach consciousness. Stimulation of the parietal cortex causes subjects to report having moved, even in the absence of actual motor responses. Parietal and premotor cortex regions are serious contenders for bringing motor intentions and motor responses into awareness. We used electrical stimulation in seven patients undergoing awake brain surgery. Stimulating the right inferior parietal regions triggered a strong intention and desire to move the contralateral hand, arm, or foot, whereas stimulating the left inferior parietal region provoked the intention to move the lips and to talk. When stimulation intensity was increased in parietal areas, participants believed they had really performed these movements, although no electromyographic activity was detected. Stimulation of the premotor region triggered overt mouth and contralateral limb movements. Yet, patients firmly denied that they had moved. Conscious intention and motor awareness thus arise from increased parietal activity before movement execution.

From eye to hand: planning goal-directed movements.

The nature of the neural mechanisms involved in movement planning still remains widely unknown. We review in the present paper the state of our knowledge of the mechanisms whereby a visual input is transformed into a motor command. For the sake of generality, we consider the main problems that the nervous system has to solve to generate a movement, that is: target localization, definition of the initial state of the motor apparatus, and hand trajectory formation. For each of these problems three questions are addressed. First, what are the main results presented in the literature? Second, are these results compatible with each other? Third, which factors may account for the existence of incompatibilities between experimental observations or between theoritical models? This approach allows the explanation of some of the contradictions existing within the movement-generation literature. It also suggests that the search for general theories may be in vain, the central nervous system being able to use different strategies both in encoding the target location with respect to the body and in planning hand displacement. In our view, this conclusion may advance the field by both opening new lines of research and bringing some sterile controversies to an end.

A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements

It is long known that the posterior parietal cortex (PPC) is critically involved in goal-directed movements. Nevertheless, there are still some controversies about its specific functions. Although most published studies have emphasised the role of PPC in sensorimotor planning processes, it has been recently suggested that PPC can also participate to on-line movement control. We studied kinematics of hand movements in a patient with a bilateral PPC lesion who exhibited no deficit in planning of her grasping movements in central vision. She was instructed to reach and grasp a cylinder presented at different locations and her motor performance was compared to that of four healthy control subjects. To address on-line control specifically, the cylinder was quickly and unexpectedly jumped, on a few trials, at movement onset, to a new location some 10 degrees (of apparent visual angle) from the original location. The patient could easily grasp stationary objects seen in foveal vision, exhibiting the same kinematic pattern as controls. Therefore, she could plan movements accurately. In response to the object jump, unlike the controls, the patient was unable to amend her ongoing movement. In this situation, she completed two distinct movements, a first one toward the initial object location and a second one toward the final object location. These results support the hypothesis that beyond a role in movement planning, PPC plays a major role in the on-line control of reach-to-grasp movements.

A parietal-premotor network for movement intention and motor awareness

It is commonly assumed that we are conscious of our movements mainly because we can sense ourselves moving as ongoing peripheral information coming from our muscles and retina reaches the brain. Recent evidence, however, suggests that, contrary to common beliefs, conscious intention to move is independent of movement execution per se. We propose that during movement execution it is our initial intentions that we are mainly aware of. Furthermore, the experience of moving as a conscious act is associated with increased activity in a specific brain region: the posterior parietal cortex. We speculate that movement intention and awareness are generated and monitored in this region. We put forward a general framework of the cognitive and neural processes involved in movement intention and motor awareness.

Normalizing motor-related brain activity Subthalamic nucleus stimulation in Parkinson disease

Objective: To test whether therapeutic unilateral deep brain stimulation (DBS) of the subthalamic nucleus (STN) in patients with Parkinson disease (PD) leads to normalization in the pattern of brain activation during movement execution and control of movement extent. Methods: Six patients with PD were imaged off medication by PET during performance of a visually guided tracking task with the DBS voltage programmed for therapeutic (effective) or subtherapeutic (ineffective) stimulation. Data from patients with PD during ineffective stimulation were compared with a group of 13 age-matched control subjects to identify sites with abnormal patterns of activation. Conjunction analysis was used to identify those areas in patients with PD where activity normalized when they were treated with effective stimulation. Results: For movement execution, effective DBS caused an increase of activation in the supplementary motor area (SMA), superior parietal cortex, and cerebellum toward a more normal pattern. At rest, effective stimulation reduced overactivity of SMA. Therapeutic stimulation also induced reductions of movement related “overactivity” compared with healthy subjects in prefrontal, temporal lobe, and basal ganglia circuits, consistent with the notion that many areas are recruited to compensate for ineffective motor initiation. Normalization of activity related to the control of movement extent was associated with reductions of activity in primary motor cortex, SMA, and basal ganglia. Conclusions: Effective subthalamic nucleus stimulation leads to task-specific modifications with appropriate recruitment of motor areas as well as widespread, nonspecific reductions of compensatory or competing cortical activity.

The effect of viewing the static hand prior to movement onset on pointing kinematics and variability

Pointing accuracy and arm movement kinematics of six human subjects were measured in three conditions where the hand was never visible during the ongoing movement: (1) in the dark; (2) the static hand was seen in peripheral vision prior to target presentation, but not during the reaction time (H−T); (3) the static hand was seen in peripheral vision until movement onset (H+T). It was shown that: (1) viewing the hand prior to movement decreased pointing variability as compared to the dark condition. (2) Viewing simultaneously hand and target (H+T) further decreased pointing variability as compared to the H−T condition. This effect was proportional to the reaction time. (3) A lengthening of the deceleration phase was observed for movements performed in the H + T condition, as compared to the other two conditions. (4) A negative correlation between variability and the first part of the deceleration phase was observed in the H + T condition, but neither in the H-T condition nor in the dark. These results suggest that the decrease in pointing variability observed in the H + T condition is due to a feedback based on kinesthetic reafference. Better encoding of the initial position of the hand relative to the target (as in H + T) would allow a calibration of arm position sense, which is used to drive the hand toward the target during the deceleration phase.

Functional anatomy of saccadic adaptation in humans

Positron emission tomography (PET) was used to investigate the neurophysiological substrate of human saccadic adaptation. Subjects made saccadic eye movements toward a visual target that was displaced during the course of the initial saccade, a time when visual perception is suppressed. In one condition, displacement was random from trial to trial, precluding any systematic modification of the initial saccade amplitude. In the second condition, the direction and magnitude of displacement were consistent, causing adaptative modification of the initial saccade amplitude. PET difference images reflecting metabolic changes attributable to the process of saccadic adaptation showed selective activation of the medioposterior cerebellar cortex. This localization is consistent with neurophysiological findings in monkeys and brain-lesioned humans.