The mental representation of hand movements after parietal cortex damage

Science

Volumn 273, Issue 5281, 1996, Pages 1564-1566

  Sirigu, Angela ^a   Duhamel, Jean René ^b   Cohen, Laurent ^c   Pillon, Bernard ^a   Dubois, Bruno ^a   Agid, Yves ^a  

^a INSERM   (France)

^b l'alimentation et l'Environnement   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; HAND MOVEMENT; IMAGE ANALYSIS; MENTAL CAPACITY; PARIETAL LOBE; PRIORITY JOURNAL; VISUAL SYSTEM; VOLUNTARY MOVEMENT;

EID: 0029778753     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.273.5281.1564     Document Type: Article

References (33)

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22. All participants gave their informed consent before taking part in this study. Nine naïve right-handed normal volunteers between the ages of 30 and 74 (mean = 49 years) participated as controls. Patients were selected on the basis of lesion location and the presence of hand movement difficulties. Lesion sites were reconstructed from magnetic resonance imaging scans and were confined to the parietal cortex. The site of lesions varied among patients and involved the superior and inferior parietal lobule in posterior parietal cortex (areas 7, 39, and 40), and more anterior lesions located in the hand representation region of the postcentral gyrus. Despite this diversity of lesion sites, all patients showed overlapping symptoms with regard to hand movement execution and motor imagery impairments, but none had visuo-spatial or attentional problems, which are frequently observed with right parietal cortex lesions. All patients but case R.L., who had a tumor, suffered a cerebro-vascular injury about 2 months before their participation in our study. None of the patients showed motor or sensory deficits, hemispatial neglect, body schema disorders, or asomatognosia at the time of testing. Patient R.K. is a 38-year-old male with a right anterior parietal lesion partially extending into the precentral gyrus. His chief complaint consisted of difficulties with differentiated movements of the left fingers. Patient J.D. is a 62-year-old woman with a right superior parietal lesion, who presented left-sided difficulties with hand movements and visually guided reaching. Patient R.L. is a 28-year-old male with left parietal astrocytoma occupying the angular and supramarginal gyri. There was a mild ideomotor apraxia, and the patient reported needing to look more carefully at his hands when manipulating objects. Simple hand movements were fast and accurate when made under visual control but deteriorated when visual feedback was removed. Patient J.J. is a 60-year-old male with a left lesion of both inferior and superior parietal lobules and presented bilateral ideomotor apraxia and manual grasping difficulties restricted to the right hand. In addition to the patients with parietal lobe lesions, we tested C.P., a 73-year-old female with a degenerative pyramidal syndrome of the left upper limb. A position emission tomography scan showed cortical hypometabolism in the middle rolandic region, corresponding to the hand representation in primary motor cortex. Her case is reported in detail elsewhere (5). The movements selected for the experimental tasks were within the range of the motor capabilities of all patients, despite the presence of a performance asymmetry between the affected contralesional and intact ipsilesional sides. It should be noted that increased movement duration, which is the only variable reported here, can be the consequence of different underlying impairments and does not imply necessarily hypokinetic behavior.
23. One potential concern is that opportunity for relearning of mental imagery could explain the dissociation of mental simulation accuracy between motor cortex and parietal damage. Most patients were followed up over an extended period of time. C.P., the patient with motor cortex damage, was first seen 3 months after onset of her motor impairments. She was tested repeatedly for over 2 years, and her performances in motor imagery tasks neither improved nor deteriorated. Patient J.J. was seen only once, shortly after his stroke; hence, we have no follow-up data on him. Patient R.L., whose tumor had been diagnosed 4 years before we began testing him, performed various mental imagery tasks on numerous occasions over a 6-month period. The impairment was quite severe and did not change over time. Quite to the contrary, the patient reported that because these experiments made him acutely aware of a deficit he did not know he had, he deliberately tried to train himself at forming mental images of hand movements but was always unsuccessful. The remaining patients had non-evolving, vascular lesions (R.K. and J.D.). Follow-up testing over a 6- to 9-month period showed no change. Therefore, it appears that the inability to form mental representations of upper limb movements appears to be a stable and permanent consequence of parietal lobe lesions.
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28. The study does not address the contribution of visual imagery to mentally simulated movements, though it has been suggested that a representation of visual context is activated in conjunction with an imagined action [S. M. Kosslyn, Image and Brain (MIT Press, Cambridge, MA, 1994)]. Because they are specific to a particular body part, it is unlikely that impairments of the type described here could result from a visual imagery deficit. Another question is whether parietal patients can generate a static representation of their hands. Mental movement simulation would be preempted without this capacity, and the apparent motor imagery impairment would in fact reduce to a selective body schema disturbance. Subjective descriptions obtained from patients ranged from an incapacity to "imagine my hand as other than normal" (R.K.) to a subjective sense of a fading image of the hand during movement (R.L.). In view of the latter comment, and given the marked motor imagery impairment exhibited by R.L., we used a modified mental rotation task [L. M. Parsons, J. Exp. Psychol. Hum. Percept. Perform. 20, 709 (1994)] to assess the capacity to form mental pictures of one's hands. Participants listened, with eyes closed, to verbal instructions asking them to imagine one of their hands in a particular position and report the side on which the little finger (or the thumb, on alternate trials) appeared from their own perspective. A typical instruction was: "Imagine your own left hand, fingers pointing down, back of the hand facing you. Is your thumb on your left or right side?" This task can be performed correctly only if the individual imagined the designated hand (left or right) in the appropriate orientation referred to his or her own point of view. R.L. scored 29/32 (91%) correct on this task, with a mean response latency of 6.2 s, within the range of the control individuals (81 to 100% correct, 3.8 to 7.8 s mean response latency). Hence, the behavior observed after parietal lesion appears to concern specifically the ability to generate a representation of hand movements, not hand shapes or orientations.
29. The study does not address the contribution of visual imagery to mentally simulated movements, though it has been suggested that a representation of visual context is activated in conjunction with an imagined action [S. M. Kosslyn, Image and Brain (MIT Press, Cambridge, MA, 1994)]. Because they are specific to a particular body part, it is unlikely that impairments of the type described here could result from a visual imagery deficit. Another question is whether parietal patients can generate a static representation of their hands. Mental movement simulation would be preempted without this capacity, and the apparent motor imagery impairment would in fact reduce to a selective body schema disturbance. Subjective descriptions obtained from patients ranged from an incapacity to "imagine my hand as other than normal" (R.K.) to a subjective sense of a fading image of the hand during movement (R.L.). In view of the latter comment, and given the marked motor imagery impairment exhibited by R.L., we used a modified mental rotation task [L. M. Parsons, J. Exp. Psychol. Hum. Percept. Perform. 20, 709 (1994)] to assess the capacity to form mental pictures of one's hands. Participants listened, with eyes closed, to verbal instructions asking them to imagine one of their hands in a particular position and report the side on which the little finger (or the thumb, on alternate trials) appeared from their own perspective. A typical instruction was: "Imagine your own left hand, fingers pointing down, back of the hand facing you. Is your thumb on your left or right side?" This task can be performed correctly only if the individual imagined the designated hand (left or right) in the appropriate orientation referred to his or her own point of view. R.L. scored 29/32 (91%) correct on this task, with a mean response latency of 6.2 s, within the range of the control individuals (81 to 100% correct, 3.8 to 7.8 s mean response latency). Hence, the behavior observed after parietal lesion appears to concern specifically the ability to generate a representation of hand movements, not hand shapes or orientations.
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33. Supported by fellowships from the French Fondation pour la Recherche Médicale and the Human Capital and Mobility program of the European Community to A.S.