1 Inserm U289 and , 2 Department of Neuroradiology, Hôpital de la Salpêtrière, Paris, , 3 Department of Medical Research, Service Hospitalier Frédéric Joliot, CEA, Orsay and , 4 Institut des Sciences Cognitives, CNRS, Lyon, France
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Abstract |
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Introduction |
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Studies using positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) techniques demonstrated that most of the regions that are active during overt movement execution, such as the parietal and premotor cortex, the basal ganglia, and the cerebellum, are active as well during mental simulation (Decety et al., 1994; Stephan et al., 1995
; Grafton et al., 1996a
). One important corollary of this idea is that movement imagination and execution share many properties, including a common neuronal circuitry (Jeannerod, 1994
, 1999
; Jeannerod and Frak, 1999
). Accordingly, we should expect that a lesion anywhere in the motor circuitry would lead to a parallel deficit for the executed and imagined movement. Indeed, it has been shown that patients with right motor cortex damage (Sirigu et al., 1995a
) and patients with basal ganglia dysfunction following Parkinson's disease (Dominey et al., 1995
) show a parallel impairment in imagined and executed movements. This suggests that the output produced in the motor and striatal pathways during motor imagery is similar to what is occurring during movement execution. Recently, however, Sirigu et al. demonstrated that patients with parietal lesions lose the ability to predict the duration of a movement through mental rehearsal, contrary to normal subjects and patients with motor cortex damage (Sirigu et al., 1996
). Moreover, patients with left parietal lesion were impaired when imagining movements of both the left and the right hand, while patients with right parietal lesion only showed an imagination deficit of the contralateral hand.
Thus, while the motor cortex and the basal ganglia do not appear critical in forming or maintaining a mental image of a limb in action, the parietal cortex, and perhaps predominantly the left parietal cortex, could be the cortical area where motor images are stored. Sirigu et al. (Sirigu et al., 1996) suggested that the parietal cortex sets up an internal model of the projected movement, and allows us to make predictions about how the movement will unfold and about its expected outcome. Following this hypothesis, we expect that imagined movements activate specific areas within the parietal cortex that are partially distinct from those involved in movement execution.
A role for the posterior parietal cortex in motor imagery has been suggested by other neuroimagery studies using tasks such as complex motor procedures (Roland et al., 1980), joystick (Stephan et al., 1995
) or grasping movements (Decety et al., 1994
; Grafton et al., 1996a
), and generation of a visual image of finger movements (Deiber et al., 1998
). However, none of these studies reported a functional specificity of parietal areas during movement imagery.
In the present study, we compared motor imagery with motor execution of hand movements. We were interested in knowing whether a specific cerebral network is involved in the mental simulation of hand movements as compared with their execution. Following the results of Sirigu et al. (Sirigu et al., 1996), we expected to find areas within the parietal cortex specifically devoted to mental movement rehearsal and a strong and predominant activation of the left posterior parietal cortex during movement imagination of both hands.
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Materials and Methods |
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We studied eight right-handed healthy volunteers (five males and three females, mean age 26.6 years, range 2135 years) at 3 T using a Bruker Whole-body Magnetic Resonance Imaging system. Subjects had no history of neurological or psychiatric disease, they were paid for their participation and gave informed consent. The experiment was approved by the local ethics committee. All subjects completed the Edinburgh Handedness Inventory and were strongly right-handed (Dellatolas et al., 1988).
Task
Subjects were required to perform one of the following tasks: execution of hand movements, imagination of the same hand movements and rest.
Movement Execution
Subjects were required to execute a simple (simultaneous flexion/ extension of the fingers) or complex (selective flexion/extension of the index and the little finger) continuous movement, as previously described (Sirigu et al., 1996).
Movement Imagination
Subjects were asked to imagine the same movements without actually performing them. EMG was recorded from surface electrodes positioned on the forearm, during rest, imagination and execution of the same simple and complex movements. Surface EMG did not detect any muscular activity during imagination and rest conditions, whereas a regular pattern of muscular activity during execution of hand movements (200600 mV signals) was detected. The ability of each subject to perform mental imagery was assessed by means of a modified version of a motor imagery questionnaire (Hall et Pongrac). Imagery scores ranged from eight (good imager) to 56 (poor imager). Subjects were considered as having good imagery abilities when their score fell between eight and 32, and those with poor imagery abilities between 33 and 56. All subjects showed good imagery abilities (mean 16.0 ± 5.4, range 1022 for visual imagery and mean 17.9 ± 7.2, range 926 for kinesthetic imagery). This questionnaire also provided the subjects with an opportunity to train themselves to the motor imagery task.
Both imagined and executed movements were externally paced at 0.5 Hz by an auditory stimulus.
Rest
Subjects were asked to stay motionless and relax. The same auditory tone was heard at the same rate as in the two other conditions.
Experimental Design
There were five different conditions: rest (R), simple imagined (SI), simple executed (SE), complex imagined (CI) and complex executed (CE). A resting period alternated with each of these experimental conditions which were randomized across eight runs. Four runs were performed with the right hand and four runs with the left hand. Each run was composed of 12 epochs, each lasting 20 s. At the beginning of each epoch an auditory sentence warned the subject of the type of task to perform in the following trials (e.g. simple executed). The advantage of this experimental design over previous studies of motor imagery is that it allowed us to perform direct comparisons both between each experimental task and with respect to the rest condition.
Functional Imaging
Twenty-four 5-mm-thick axial slices were obtained with a T2* weighted gradient echo, echo planar imaging sequence, using blood oxygen leveldependent contrast (repetition time 5000 ms, echo time 40 ms, flip angle of 90°, matrix 64 x 64, field of view 220 x 220 mm2). Fifty-two brain volumes were acquired for each run (four volumes for each of 13 epochs). The first four volumes of each run were discarded to reach signal equilibrium. Subsequently to the functional protocol, high-resolution three-dimensional anatomical images of the whole brain were also acquired (gradient-echo inversion recovery, repetition time 1600 ms, echo time 5 ms, matrix 256 x 256, field of view 220 x 220 mm2).
Statistical Analysis
All data were performed with Statistical Parametric Mapping (SPM 96, Wellcome Department of Cognitive Neurology, London, UK). For each subject, anatomical images were transformed stereotactically to Talairach coordinates using the standard template of the Montreal Neurological Institute. The functional scans, corrected for subject motion, were then normalized using the same transformation and smoothed with a Gaussian spatial filter to a final smoothness of 5 mm. Data were analyzed on an individual (subject per subject) basis and across subjects (group analysis) using across subjects variance (random effect analysis) (Friston et al., 1999). For individual analysis, data from each run were modeled using the general linear model with separate functions modeling the hemodynamic response to each experimental epoch, leaving 211 degrees of freedom per subject analyses. Covariates were used to model long-term signal variations (temporal cut-off 240 s) and overall differences between runs. Six contrasts were defined as follows: (i) execution of hand movements compared with rest; (ii) imagination of hand movements compared with rest; (iii) execution compared with imagination of hand movements; (iv) imagination compared with execution of hand movements; (v) complex compared with simple movements; and (vi) simple compared with complex movements. The absence of interaction between the imagined/executed factor and complex/simple factor was also assessed. As left and right movements were performed in separate runs, which does not allow for the differentiation of the inter-run from the leftright effects, the left versus right comparison were not assessed. Data for each hand were pooled for statistical comparisons. Statistical parametric maps were calculated for each contrast. We first thresholded the Z maps at Z = 3.09 (P < 0.001). In these thresholded maps, activated clusters were considered significant if their spatial extent was >18 voxels (or 172 mm3), corresponding to a risk of error (type I error) of P < 0.05. For group analysis, parametric maps were constructed using the same threshold and the same contrasts as for the subject per subject analysis. For the basal ganglia study, a more liberal statistical threshold (P < 0.01) uncorrected for multiple comparison was used because for these structures multiple comparison correction for the entire volume of the brain would lead to a much too high risk of type II error (the risk of accepting the null hypothesis when it should be rejected). For small structures, such as the putamen, the thalamus and the caudate nucleus, this threshold is valid because the statistical analysis is guided by a very strong anatomical hypothesis, with well-defined and invariant anatomical landmarks across subjects.
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Results |
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Execution of Movement Compared with Rest
Significant signal changes were found in the primary sensorimotor, the medial and lateral premotor areas, the superior and inferior parietal areas, the basal ganglia, the thalamus and the cerebellar hemispheres bilaterally (Table 1 and Figure 1
).
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In the parietal lobe, activation was located in the primary sensory areas (SI), which correspond to BA 13, and in the parietal operculum (SII), which corresponds to the opercular part of BA 40 and 43. Activation was also found in the rostral part of the superior parietal regions bilaterally (BA 7) and in the left postero-inferior parietal area (BA 40).
In the basal ganglia, the putamen was arbitrarily divided into an anterior and a posterior area using the VCA line as a landmark. Activation was observed in both the anterior and posterior parts of the putamen, bilaterally. Bilateral activation was also found in the ventrolateral nucleus of thalamus and in the rostral part of the cerebellar cortex.
Imagination of Movement Compared with Rest
When imagination was directly compared with rest (Table 1 and Figure 1
), activation included bilateral medial and lateral PM areas, superior and inferior parietal areas and basal ganglia.
When contrasted with the execution condition, no activation was found in the right or left primary motor areas, while other newly activated regions were observed.
The frontal lobes showed activation in the left dorsolateral prefrontal area (BA 9 and 46) and in the right rostral prefrontal area (BA 10 and 11).
In the parietal lobe, a large activation of the superior areas (BA 7) was observed, extending more caudally (y coordinate of maximal Z value = 54 and 60 in the right and left hemispheres, respectively) than those activated during executed movements (y coordinate of maximal Z value = 36 and 42 in the right and left hemispheres, respectively). Significant activation was also detected in the rostral area 40 of the inferior parietal lobe close to the post-central gyrus, whereas no activation was found in the ventral inferior parietal area (BA 40 and 43).
In the basal ganglia, the activation sites were located more rostrally than those described during movement execution. The caudate nucleus and the anterior part of the putamen were activated during mental simulation, whereas no activation was found in the posterior part of the putamen.
The middle part of the left temporal lobe (BA 21) and bilateral inferior frontal areas (BA 44/45) were also activated.
Execution Compared with Imagination of Movement
The direct comparison between executed and imagined movement showed a significant network of activation, centered on the central sulcus (Table 2, Figures 1 and 2
). This network included, bilaterally, the sensorimotor and the lateral PM cortex, the post-SMA and the anterior cingulate cortex (BA 24), and the ventral inferior parietal areas (BA 40 and 43).
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Areas activated during imagined movements surrounded the activation sites observed during the executed movements, being more rostral in the frontal lobes and more superior and caudal in the parietal cortex (Table 2, Figures 1 and 2
). Activation was particularly important in the superior and inferior parietal cortex (BA 7, 40), the prefrontal cortex (BA 46, 9 and 10, 11), and the pre-SMA. The frontal lobe also showed activation in the lateral PM cortex bilaterally and in the right anterior cingulate cortex (BA 32). Activation in the parietal lobes was left-sided (BA 7 and 40).
Significant activation in the middle temporal area and the caudal inferior frontal cortex (BA 44) was also detected.
In the basal ganglia, activation was rostral to the VCA line. The anterior part of the putamen was activated in the left hemisphere, whereas the head of the caudate nucleus was activated in the right hemisphere though with a lower threshold (P = 0.01, non-corrected). No activation was detected in the thalamus or the cerebellum (Figure 3).
Complex Movements Compared with Simple Movement
The comparisons between complex and simple movement, and between simple and complex movements showed no significant activation.
Results in Individual Subjects
Analysis of individual data is presented in Table 3. Individual analysis allowed us to study inter-subject variability of activated areas as well as the correspondence between anatomy and activation, which was of particular interest in the parietal lobe, the SMA and the basal ganglia.
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In the SMA, when comparing imagination with execution and execution with imagination, the group pattern was seen in all eight subjects (Figure 4). Activation observed during imagination of movement was located in the pre-SMA while during execution in the post-SMA. Only one subject showed activation in the post-SMA during imagination, although the pre-SMA was more significantly activated in the same subject (pre-SMA: Z = 7.50 and 7.56; post-SMA: Z = 6.22 and 6.75 in the left and right hemispheres, respectively). In addition, when each experimental task (imagination and execution) was contrasted to the rest condition, a rostro-caudal gradient was found in the post-SMA, in two and six out of the eight subjects in the right and the left hemispheres, respectively. Therefore, the caudal part of the post-SMA was more specifically involved during execution and the rostral part during imagination (mean y during execution: right = 7.2 and left = 6.54; and imagination: right = 6 and left = 3, Student's t-test, P < 0.05).
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In the parietal lobe, the individual results confirmed the existence of a functional dissociation between the areas involved in motor imagery and those implicated in motor execution (Table 3). During imagination, activation was restricted to the caudal part of the superior and inferior parietal regions (BA 7 and 40), while actual execution was associated with more rostral and bilateral activation in the inferior and the superior parietal lobe (SI and SII areas). Anatomically, the posterior parietal area, which was more activated during imagination, was divided into a superior and an inferior region. The superior region corresponded to BA 7 close to the posterior part of the intra-parietal sulcus. The post-central sulcus, the lateral and the horizontal part of the intra-parietal sulcus limited the inferior region. We also identified anatomically the regions more activated during actual execution of movement. SI area extended from the posterior bank of the central sulcus to the post-central sulcus (BA 1, 2, 3). SII was located in the depth of the Sylvian fissure and the opercular area, bounded rostrally by the central sulcus (BA 40 and 43).
Interestingly, activation in the parietal cortex during imagination largely predominated in the left hemisphere (Figure 4). All subjects but one presented a focus of activation located in the left inferior parietal cortex, whereas only two had a similar activation in the homologous region of the right hemisphere with a lower statistical significance than in the left hemisphere. In the superior parietal cortex, one subject activated the left hemisphere only and five out of eight subjects presented foci of activation in both hemispheres, with a higher statistical significance on the left side (mean Z score across subjects = 6.32 ± 0.99 and 5.19 ± 1.71 in the left and right hemispheres, respectively, P = 0.03, Student's t-test). During movement execution, both parietal lobes were activated symmetrically.
Analysis of individual data showed that distinct subcortical structures were involved when executed and imagined movements were compared with rest. During imagination, there was a prominent activation located in the head of the caudate nucleus and the anterior part of the putamen, whereas during movement execution activation was mainly found in the anterior and posterior parts of the putamen (Table 3). Therefore, the caudate nucleus was more specifically activated during motor imagery whereas the posterior part of the putamen was more specifically activated during the actual performance of the movement, and the anterior part of the putamen was equally activated in both conditions. Activation in the caudate nucleus during movement imagination was associated with prefrontal activation in seven out of eight subjects.
The comparison between complex and simple movements showed a significant number of foci in the parietal cortex, and fewer in the premotor cortex (Table 3). In the parietal lobes, activation in the primary sensory area was observed in six and four subjects in the right and left hemispheres, respectively. Activation in the posterior parietal areas was largely predominant in the left hemisphere (one in the right, six in the left). Thus, the left parietal cortex was more specifically activated during complex movements. The comparison between simple and complex movements was not associated with any significant increase of regional cerebral blood flow.
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Discussion |
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However, when imagination was directly compared with execution a specific circuit underlying motor imagery was found. Imagination of movement involved rostral premotor and prefrontal areas and caudal regions in the parietal cortex, whereas execution was predominantly associated with activation in areas located around the central sulcus. Likewise, in the basal ganglia, activation in the head of the caudate nucleus was more closely associated with motor imagery while the posterior part of the putamen was mainly involved in motor execution. As expected, we found a predominant role of the left posterior parietal cortex during mental simulation.
Thus, our results show a shift of the metabolic signal along an antero-posterior gradient within the parietal lobe and along a postero-anterior gradient within the frontal cortex from execution to imagination of a movement.
Parietal Cortex
One of the main findings of the present study was that functionally distinct regions of the parietal lobes subserved execution and imagination of hand movements. The primary (BA 1, 2, 3) and secondary sensory areas (SII, BA 40 and 43) were more activated during the execution of movement, whereas both the superior and the inferior parietal cortex (BA 7 and 40) were more closely associated with imagination.
Activation in the posterior parietal regions obtained in the comparison of imagination with rest is in agreement with previous data on cerebral activation during hand movement. Several imaging studies have reported an activation in the superior (BA 7) or inferior parietal lobules (BA 40) in subjects performing motor imagery tasks (Decety et al., 1994; Stephan et al., 1995
; Grafton et al., 1996a
). However, none of these studies demonstrated additional activation in parietal areas during imagination with respect to execution.
The specific role of the parietal cortex in movement ideation which emerges here is consistent with neuropsychological studies. Left parietal lobe lesions produce apraxia, an impairment of skilled movements, in the absence of elementary sensory or motor deficits. Patients with apraxia have difficulties in performing hand movements, such as symbolic gestures (DeRenzi et al., 1982) and object pantomimes, that need to be guided by internal representations (Clark et al., 1994). Parietal lesion can affect both motor production and ideation, since these patients are also unable to recognize the meaning of gestures (Heilman et al., 1982
; Sirigu et al., 1995b
). Recently, Sirigu et al. (Sirigu et al., 1996
), using different hand motor tasks, showed that parietal-lesioned patients were unable to match their actual movement duration during mental imagery, suggesting that what might be altered in these patients is an internal representation of learned manual motor synergies. Thus, the parietal cortex could play a crucial role in the generation of mental motor images (Sirigu et al., 1996
). The results of the present study further corroborate the neuropsychological data and provide, at least for the type of movements studied here, anatomical evidence for the existence of areas within the parietal lobe specifically devoted to movement imagery.
An important aspect of the parietal involvement in movement imagery is the predominant role of the left parietal lobe. Only the left, but not the right, parietal lobe was more activated during imagination compared with execution of both right and left hand movements. To our knowledge, such a predominance of the left parietal lobe in motor imagery has not been reported in previous fMRI studies. This result is in accordance with previous studies which showed that only lesions of the left parietal lobe can produce bilateral apraxia (De Renzi et al., 1982; Heilman et al., 1982
) and motor imagery impairment for both hands (Sirigu et al., 1996
). The predominance of the left parietal lobe activation was also found to be associated with movement complexity.
Two parietal areas were more activated during movement execution than during imagery: the primary sensory areas and the parietal operculum. The primary sensory areas were activated in all subjects during execution and imagination (when these two conditions were compared with rest), in agreement with a recent fMRI study (Porro et al., 1996). Activation of SI may reflect sensory feedback processes. The lack of activation in SI during imagery (compared with execution) suggests that this area was not essential for mental simulation. An additional area located in the parietal operculum was activated only during execution. This area may correspond to the second somatosensory area (SII). In monkeys, microstimulation in this region trigger contralateral limb and head movements (Mori et al., 1985
). A previous PET study (Grafton et al., 1996b
) showed that SII activation was significantly greater during grasping than pointing, suggesting that SII may play a role in the tactile exploration of objects. SII activation has also been observed during simple self-paced hand movement (Lehéricy et al., 1998
), suggesting that it may be involved in even more simple aspects of sensory control.
Lastly, when comparing complex and simple movements by combining both task conditions (execution and imagination), individual subjects' analysis showed a significant number of activation foci in the parietal cortex (primary sensory and posterior parietal areas). The specific involvement of the parietal cortex for complex movements is in line with a previous PET study which showed that in normal subjects the execution of a sequential finger movement increasing in complexity is associated with a growing metabolic signal within these areas (Catalan et al., 1998). Our findings are also in agreement with the results obtained in patients with parietal lesions who showed a more severe impairment in mentally imagining complex movements rather than simple ones (Sirigu et al., 1996
). Thus, the parietal cortex may contribute to the integration of sensory information into the ongoing movement or to an important attentional recruitment associated with complex movements (Jenkins et al., 1994
).
Frontal Cortex
Primary Motor Area
During movement execution the primary motor cortex was constantly activated in the region known as the hand area (Yousry et al., 1997). In contrast, no activation was observed in the primary motor cortex when imagination was compared with execution. However, individual subject analysis showed that four out of the eight subjects significantly activated this region when imagination was compared with rest. The activity in M1 during movement imagination was not related to muscular contractions, as no consistent increase of EMG activity response was recorded during imagination (see Materials and Methods). These data suggest that M1 does not play a predominant role in motor imagery, although it may be activated in individual subjects. These findings are consistent with recent imaging studies, which reported a less significant activation of M1 during imagined than actual movements in control subjects (Lang et al., 1996
; Porro et al., 1996
; Roth et al., 1996
; Schnitzler et al., 1997
). They are also in line with studies in patients, which showed that imagination of movement was not impaired in patients with motor cortical damage (Sirigu et al., 1995a
).
Supplementary Motor Area
In our study, the SMA showed two functional subdivisions. First, in the post-SMA, we found a rostro-caudal gradient between imagined and executed movement. This pattern was restricted to the left hemisphere in individual subject analysis. Second, the pre-SMA was more specifically involved in imagination of movement.
A functional subdivision of the post-SMA for real and virtual movements has already been reported (Tyszka et al., 1994; Stephan et al., 1995
; Grafton et al., 1996a
). In monkeys, area F3, which is considered to be the homologue of the post-SMA, is strongly connected with superior parietal areas (Rizzolatti et al., 1998
). Thus, the left-lateralized activation within the post SMA observed during motor imagery may be related to the left dominant activation we also found in the superior parietal lobe.
Previous reports have shown that the preand post-SMA are activated differentially during motor tasks depending on the type of movements, with the pre-SMA more involved in the selection (Deiber et al., 1992) and preparation of movement (Humberstone et al., 1997
) while the posterior part is more active during execution (Deiber et al., 1992
; Stephan et al., 1995
; Lehéricy et al., 1998
) and movements initiation (Passingham, 1997
). The present data suggest a role of the pre-SMA in movement imagination.
Thus, the supplementary motor area consisted of three distinct functional areas: the pre-SMA, which plays a role in motor control at a high representational level; the rostral part of the post-SMA, which is also implicated in motor imagination; and the caudal part of the post-SMA, which is more closely tied to motor execution. The anatomical subdivision of this functional architecture was provided by a recent cytoarchitectonic study (Vorobiev et al., 1998).
Premotor and Prefrontal Cortex
In the lateral premotor cortex, a rostro-caudal gradient similar to the one found in the SMA was observed in most of the subjects as well as in the group data. Previous studies have already reported lateral premotor activation during movement imagination (Rao et al., 1993; Decety et al., 1994
; Stephan et al., 1995
). Stephan et al. (Stephan et al., 1995
) suggested that activation of the anterior part of the premotor cortex might be more important during imagination rather than execution, although they did not find such a gradient in the direct comparison of the two experimental conditions. In humans, the posterior part of the premotor cortex (BA 6) may correspond to areas F2 and F4 in the monkey, which send direct outputs to the spinal cord (Rizzolatti et al., 1998
). These data are in a good agreement with the functional specificity of the posterior area 6 during the execution of movement. On the other hand, the anterior part of the premotor cortex may correspond to areas F5 and F7 in the monkey, which do not project to the spinal cord. This area, in association with the anterior cingulate cortex, may be involved in cognitive aspects of motor processes such as movement imagination, as our data suggest, movement selection (Deiber et al., 1992
) or suppression of a motor response (Krams et al., 1998
).
Activation in BA 44 was observed in most of the subjects, and has been described previously during imagination of grasping (Grafton et al. 1996a). This region, which seems to be the homologue of area F5 in monkeys, may play a role during both imagination and execution of hand movement, as our data seem to suggest. Activation in BA 45 was found during the observation of a hand movement (Grafton et al., 1996a
; Rizzolatti et al., 1996
; Decety et al., 1997
), suggesting that BA 45 also plays a role in action recognition.
Lastly, group data, as well as individual subject analysis, showed activation in the lateral prefrontal cortex mainly during imagination (BA 9, 10, 11 and 46). Previous neuroimagery studies in humans have shown that the dorsal prefrontal cortex is activated when the subject has to make a decision, such as which finger to move (Frith et al., 1991) or when to start a finger movement (Jahanshahi et al., 1995
). In monkeys, the area F6 is strongly connected with the dorsolateral prefrontal cortex (Luppino et al., 1993
). These data are consistent with the fact that these two areas were both activated during movement imagination.
Frontal and Parietal Activation: a Functional Loop for Hand Movement Representation?
The conjunction of premotor and parietal cortex activation during motor imagery is consistent with anatomical data. In monkeys, the intraparietal sulcus is richly connected to the premotor cortex (Johnson et al., 1996; Matelli et al., 1998
). Neurophysiological studies show matching patterns of neuronal activity within the parietal and the frontal cortex. Chafee and Goldman-Rakic have demonstrated that during an oculomotor delayed task, response profiles in both the parietal and the frontal regions showed comparable temporal duration and spatial tuning (Chafee and Goldman-Rakic, 1998
). In a more recent study, the same authors have showed that inactivation by cooling the parietal cortex changed significantly the activity of frontal neurons during the cue, the delay and the saccade period. Likewise, inactivation of the prefrontal cortex equally affected the behavior of parietal neurons (Chafee and Goldman-Rakic, 2000
). Although exact homologies between the parietal and frontal regions of monkeys and humans are not yet fully established, it is reasonable to assume that, as in monkeys, the human parietal and frontal areas are organized as a tightly coupled functional system with highly specific connections between their respective anatomical subdivisions. Parietal areas could constitute the neural substrate for the storage of visual and kinesthetic limb postures, and for mapping these representations onto the premotor and motor regions which contain the corresponding motor programs (Sirigu et al., 1996
). Through reciprocal connections, the movement forms activated in the posterior parietal cortex by a visual stimulus (or by mental imagery) can be interpreted as a particular motor action via the activation of premotor cortical neurons such as the mirror neurons described by Rizzolatti and his co-workers in area F5 of the premotor cortex (Di Pellegrino et al., 1992
; Gallese et al., 1996
; Rizzolatti et al., 1998
).
The metabolic gradient we describe here within the fronto-parietal network is similar to what has been described by neurophysiological studies in the monkey's brain. Premotor and parietal regions contain neurons with both motor and sensory properties organized along a gradient, following a sensory-to-motor rostro-caudal representation in the lateral premotor cortex and a motor-to-sensory rostro-caudal gradient in the superior parietal cortex (Johnson et al., 1996) [for a review see (Wise et al., 1997
)]. On the basis of these neurophysiological findings, Burnod et al. (Burnod et al., 1992
, 1999
) recently proposed a computational model of this fronto-parietal circuit composed of neurons arranged into a single layer around three main axes: visualsomatic, positiondirection and sensory motor. According to the authors, these properties reflect the computation performed by local networks. This conceptual framework presents a striking parallel with the results of the present study, and suggests that a purely representational activity (motor imagery) weighs more heavily the contribution of the portions of the sensorimotor network which are concerned with movement ideation and planning, while motor execution weighs more heavily the contribution of the regions within the network which are closest to the motor output.
Basal Ganglia
Comparing imagination and execution of hand movements revealed functional differences in the basal ganglia. During real movements, activation was mainly found in the postcommissural portion of the putamen, as previously reported (Jueptner et al., 1997; Lehéricy et al., 1998
). In non-human primates, this part of the striatum constitutes the sensorimotor territory (Alexander et al., 1986
; Albin et al., 1989
; Brooks, 1995
; Parent and Hazrati, 1995
) and receives afferents from the primary sensory motor cortex. In contrast, movement simulation activated a more rostral area in the head of the caudate nucleus, which receives afferents from the dorsolateral prefrontal cortex and is considered to be part of the associative region of the striatum. Thus, execution and imagination in the basal ganglia engaged different areas belonging to two distinct functional cortico-subcortical loops, sensori-motor and cognitive respectively, as described in monkeys (Kunzle, 1975
; Alexander et al., 1990). However, these results were obtained using a lower statistical threshold (P < 0.01) and thus need to be confirmed in a larger number of subjects.
Activation was also present in the ventrolateral part of the thalamus, which receives pallidal, cerebellar and somesthesic inputs, and projects back to the motor cortex and the supplementary motor area.
The role of the caudate nucleus in motor imagination remains to be determined. Activation in the caudate nucleus has been reported previously during mental simulation of grasping (Decety et al., 1994) and explicit learning of a sequence of key-presses (Jueptner et al., 1997
). However, disruption of the nigro-striatal dopaminergic system in patients with Parkinson's disease does not alter motor imagery, as they simulate movements as slow as actual ones (Dominey et al., 1995
). Thus, the contribution of the basal ganglia, though important in movement representation, is perhaps not instrumental in the generation of motor images.
In conclusion, our results show that, although imagination and execution of hand movements activate a large overlapping network of cerebral areas, a number of cortico-subcortical regions are more specifically devoted to hand motor imagery. These areas may constitute an important circuit for anticipating or predicting the sensory consequences of the movement. A question that now arises is why motor imagery mechanisms may have evolved this way. A possible speculation is that these neural mechanisms may have evolved in parallel with the motor preparation system to optimize learning of difficult motor tasks. When we are going to do something risky or potentially harmful, rehearsing the action allows us to try out different possibilities and may help deciding on the better strategy, when we cannot afford to go by trial and error. Such a system would in this case be essential for our survival.
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Notes |
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Address correspondence to Dr Angela Sirigu, Institut des Sciences Cognitives, CNRS, 67, Blv. Pinel, F-69675 Bron, France. Email: sirigu{at}isc.cnrs.fr.
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