Analogical transfer in sequence learning. Human and neural-network models of frontostriatal function.
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Biomedical subjects
Publications and source records attributed to M Jeannerod.
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This study was designed to investigate mentally simulated actions in a virtual reality environment. Naive human subjects (n = 15) were instructed to imagine themselves walking in a three-dimensional virtual environment toward gates of different apparent widths placed at three different apparent distances. Each subject performed nine blocks of six trials in a randomised order. The response time (reaction time and mental walking time) was measured as the duration between an acoustic go signal and a motor signal produced by the subject. There was a combined effect on response time of both gate width and distance. Response time increased for decreasing apparent gate widths when the gate was placed at different distances. These results support the notion that mentally simulated actions are governed by central motor rules.
We examined seven right-handed, asymmetrical (right side affected) Parkinson's disease patients and seven age-matched controls in a manual finger sequencing test using left and right hands in vision, no vision, and motor imagery conditions. All patients displayed motor asymmetry, favoring the left hand. They also displayed motor imagery asymmetry, mentally simulating movement more slowly with their right affected hand than with their left hand. Additionally, impairment in mental hand rotation correlated significantly with the imagery asymmetry. These data support two related hypotheses: (a) Motor sequence imagery and execution share common neural structures. (b) The frontostriatal system is among these shared structures.
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The working hypothesis of the paper is that motor images are endowed with the same properties as those of the (corresponding) motor representations, and therefore have the same functional relationship to the imagined or represented movement and the same causal role in the generation of this movement. The fact that the timing of simulated movements follows the same constraints as that of actually executed movements is consistent with this hypothesis. Accordingly, many neural mechanisms are activated during motor imagery, as revealed by a sharp increase in tendinous reflexes in the limb imagined to move, and by vegetative changes which correlate with the level of mental effort. At the cortical level, a specific pattern of activation, that closely resembles that of action execution, is observed in areas devoted to motor control. This activation might be the substrate for the effects of mental training. A hierarchical model of the organization of action is proposed: this model implies a short-term memory storage of a 'copy' of the various representational steps. These memories are erased when an action corresponding to the represented goal takes place. By contrast, if the action is incompletely or not executed, the whole system remains activated, and the content of the representation is rehearsed. This mechanism would be the substrate for conscious access to this content during motor imagery and mental training.
The physiological basis of mental states can be effectively studied by combining cognitive psychology with human neuroscience. Recent research has employed mental motor imagery in normal and brain-damaged subjects to decipher the content and the structure of covert processes preceding the execution of action. The mapping of brain activity during motor imagery discloses a pattern of activation similar to that of an executed action.
Pointing accuracy of six human subjects was measured in two blocked conditions where the hand was either never visible (T: target only) or only visible in static position prior to movement onset (H+T: hand+target). It was shown in condition H+T that, viewing the hand prior to movement greatly decreased end-point variability compared with condition T. This effect was associated with a significant modification of the movement kinematics: the H+T condition induced a shortened acceleration phase with a corresponding lengthened deceleration phase, compared with the T condition. These results led us to the hypothesis that viewing the hand prior to movement onset allowed a decrease of pointing variability through a feedback process. This hypothesis was further tested by turning the target off during the deceleration phase of the movement at half peak velocity. It was shown that turning the target off had no effect upon the T condition but induced a significant increase of pointing variability in the H+T condition. This result suggests that vision of the static hand enhances the proprioceptive localization of the limb and allows for a better visual to kinesthesic feedback.
Grasping requires coding of the object's intrinsic properties (size and shape), and the transformation of these properties into a pattern of distal (finger and wrist) movements. Computational models address this behavior through the interaction of perceptual and motor schemas. In monkeys, the transformation of an object's intrinsic properties into specific grips takes place in a circuit that is formed by the inferior parietal lobule and the inferior premotor area (area F5). Neurons in both these areas code size, shape and orientation of objects, and specific types of grip that are necessary to grasp them. Grasping movements are coded more globally in the inferior parietal lobule, whereas they are more segmented in area F5. In humans, neuropsychological studies of patients with lesions to the parietal lobule confirm that primitive shape characteristics of an object for grasping are analyzed in the parietal lobe, and also demonstrate that this 'pragmatic' analysis of objects is separated from the 'semantic' analysis performed in the temporal lobe.
Brain activity was mapped in normal subjects during passive observation of the movements of an 'alien' hand and while imagining grasping objects with their own hand. None of the tasks required actual movement. Shifting from one mental task to the other greatly changed the pattern of brain activation. During observation of hand movements, activation was mainly found in visual cortical areas, but also in subcortical areas involved in motor behaviour, such as the basal ganglia and the cerebellum. During motor imagery, cortical and subcortical areas related to motor preparation and programming were strongly activated. These data support the notion that motor learning during observation of movements and mental practice involves rehearsal of neural pathways related to cognitive stages of motor control.
Goal-directed movements imply that the visual coordinates in which the localisation of the goal is coded are transformed into proprioceptive coordinates in which the arm movement is coded. The two systems of coordinates are normally superimposed. Using a virtual reality device attached to the subject's head, we have created a situation where these systems were dissociated from each other. The virtual environment involved virtual visual targets and an image of the subject's hand reconstructed from the output of a data glove wore by the subject's right hand. When the subject's head was rotated, the visual targets and the image of the hand rotated by the same amount. Movements of the real hand were thus in conflict with those of the reconstructed hand, which appeared to err in the direction of head rotation. Pointing movements directed at five targets (0 degree, 26 degrees and 52 degrees on each side) were studied for five different head positions (0 degree, 45 degrees and 80 degrees to the right and to the left). The results showed a significant pointing bias towards head position, except for the left-most targets in the right head rotations. Constant errors in azimuth were proportional to the amount of head rotation. When the head was rotated to the right, constant errors in azimuth were greater during pointing towards right than left targets. Similarly, they were greater for left than for right stimuli when the head was rotated to the left. Errors in amplitude were not influenced by the direction nor the amount of head rotation.(ABSTRACT TRUNCATED AT 250 WORDS)
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) and 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.
The observation of a patient (A.T.) with a bilateral posterior parietal lesion of vascular origin is reported. A.T. presented a bilateral (more marked on the right) deficit in grasping simple objects (neutral cylindrical dowels) without deficit in reaching toward the location of these objects. The major symptom was an exaggerated anticipatory opening of the fingers with poor correlation with object size, resulting in awkward grasps. It was present both when the hand was visible to the subject and when it was not. This deficit was much less marked if the neutral objects were replaced by usual objects of the same sizes. Finally, in tasks where she had to indicate with her fingers the size of visual objects presented as virtual images through a mirror, or the size of imagined usual objects, A.T. performed normally. These results are discussed within the framework of a dual representation of objects. Only the "pragmatic" representation for steering object-oriented actions would be impaired in this patient as a result of posterior parietal damage. By contrast the semantic representation for object identification would be intact.
Two experiments are reported that examined the act of prehension when subjects were asked to grasp with their thumb and index finger pads an elongated object resting horizontally on a surface and placed at different orientations with respect to the subject. In Experiment 1, the pad opposition preferences were determined for the six angles of orientation examined. For angles of 90 degrees (object parallel to frontal plane) or less, no rotation of the wrist (pronation) was used; for angles 110 degrees or greater, pronation was systematically employed to reorient the finger opposition space. Only one angle, 100 degrees , produced any evidence of ambiguity in how to grasp the object: Approximately 60% of these grasps involved pronation and 40% did not. Using the foregoing grasp preference data, in Experiment 2 we examined the kinematics of the wrist and elbow trajectories during prehension movements directed at an object in different orientations. Movement time, time to peak acceleration, velocity, and deceleration were measured. No kinematic differences were observed when the object orientation either required (110 degrees ) or did not require (80 degrees ) a pronation. By contrast, if the orientation was changed at the onset of the movement, such that an unpredicted pronation had to be introduced to achieve the grasp, kinematics were affected: Movement time was increased, and the time devoted to deceleration was lengthened. These data are interpreted as evidence that when natural prehension occurs, pronation can be included in the motor plan without affecting the movement kinematics. When constraints are imposed on the movement execution as a consequence of a perturbation, however, the introduction of a pronation component requires kinematic rearrangement.
The hypothesis of several subsystems for processing visual information is expanded to the context of visuomotor functions. It is proposed that object-oriented actions involve three main types of processing whether the object is to be localized, identified, or grasped and manipulated. Neurological evidence from patients is provided, showing that each type of processing pertains to a distinct pathway. Whereas identification is impaired by lesions affecting the occipitotemporal pathway, localization and grasping are processed in posterior parietal cortex. A new clinical case with a parietal lesion is presented, where the grasping deficit contrasted with preservation of both identification and localization. This result suggests separate representations for localizing and grasping within parietal cortex.
1. Healthy subjects actually performed and mentally simulated a leg exercise at two levels of work (15 and 19 kg loads). Heart rate, respiration rate and end-tidal PCO2 were measured in both conditions. In addition, muscular metabolism was simultaneously measured using 31P nuclear magnetic resonance (NMR) spectroscopy. 2. During actual exercise, heart and respiration rates increased, first abruptly and then gradually in relation to the level of work. End-tidal PCO2 was unaltered. NMR spectra showed a drop in phosphocreatine (PCr) and an increase in inorganic phosphate (Pi) concentrations. Intracellular pH fell to 6.65 at maximal effort with a 19 kg load. 3. During mental simulation, both heart and ventilatory rate increased immediately after mental exercise was begun. This increase was proportional to the amount of simulated exercise. Heart rate remained about 25% below the level observed during actual exercise. The increase in respiration rate, by contrast, was more marked than during actual exercise. Finally, end-tidal PCO2 decreased progressively to about 18% of the resting value. 4. During mental simulation, NMR spectra were unchanged with respect to the resting values. 5. Subjects rated their sensation of fatigue using an analog rating scale, during both actual exercise and mental simulation. During mental exercise, the sensation of fatigue was greater with the 19 kg load than with the 15 kg load. 6. These results demonstrate that mental simulation of action can activate heart and respiration control mechanisms. They suggest that autonomic activation during imagined action pertains to the more general phenomenon of preparation for action.
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Measurement of cardiac and respiratory activity during mental simulation of locomotion at increasing speed revealed a covariation of heart rate and pulmonary ventilation with the degree of imagined effort. The degree of vegetative activation of a subject mentally running at 12 km/h was comparable to that of a subject actually walking at 5 km/h. This effect cannot be explained by an increase in peripheral (e.g. muscular) metabolic demands. Indeed, oxygen uptake decreased during motor imagery. This finding is suggestive of a commonality of neural structures responsible for mental imagery of movement and those responsible for programming actual movement. In addition, it provides an quantifiable way of testing mental imagery in relation to movement by using easily accessible biological markers.
Prehension involves processing information in two hypothesized visuomotor channels: one for extrinsic object properties (e.g., the spatial location of objects) and one for intrinsic objects properties (e.g., shape and size). The present study asked how the two motor components that correspond to these channels (transport and grasp, respectively) are related. One way to address this question is to create a situation where unexpected changes occur at the input level of one of the visuomotor channels, and to observe how the movement reorganizes. If transport and grasp are independent components, then changing the object location, for example, should affect only the transport, not the grasp component. Subjects were requested to reach, grasp and lift as accurately as possible one of three dowels using the distal pads of the thumb and index finger. On certain trials, upon movement initiation towards the middle dowel, the dowel was made to instantaneously change its location to one of the two other positions, requiring the subject to reorient the hand to the new dowel location. Results consisted of comparing the movement characteristics of the transport and grasp components of these perturbed movements with appropriate control movements. Kinematics of the wrist trajectory showed fast adjustments, within 100 ms, to the change of dowel position. This duration seems to correspond to the minimum delay required within the visuomotor system for visual and/or proprioceptive reafferents to influence the ongoing movement. In addition, these delays are much shorter than has been found for conditions where object location changes before movement initiation (approximately 300 ms). The faster times may relate to the dynamic character of the deviant limb position signals, with the only constraint being the physiological delays for visual and kinaesthetic signals to influence the movement. A spatiotemporal variability analysis of the movement trajectories for non-perturbed trials showed variability to be greatest during the acceleration part of the movement, interpreted as due to control by a relatively inaccurate directional coding mechanism. Control during the deceleration phase, marked by low trajectory variability, was seen to be due to a sensorimotor process, using motor output signals, and resulting in an optimized trajectory supporting a successful grasp. Analysis of the grasp component of prehension showed that perturbing object location influenced the movement of the fingers suggesting a kinematic coupling of the two components. However, forthcoming work shows that, when object size changes, and location remains constant, there is a clear temporal dissociation of the two components of prehension.(ABSTRACT TRUNCATED AT 400 WORDS)