1 Service Hospitalier Frédéric Joliot, Department of Medical Research, CEA, Orsay and IFR 49, , 2 Department of Neuroradiology, Hôpital C. Nicolle, Rouen and , 3 Department of Neuroradiology, , 4 Department of Neurology, , 5 Department of Inserm EPI 007 and , 6 Department of Biostatistics and Medical Informatics, Hôpital de la Salpêtrière, Paris, France
Address correspondence to Dr Stéphane Lehéricy, Service de Neuroradiologie, Bâtiment Babinski, Hôpital de la Salpêtrière, 47 Bd de lHôpital, 75651 Paris Cedex, France. Email: stephane.lehericy{at}psl.ap-hop-paris.fr.
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Abstract |
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Introduction |
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Improved knowledge of the organization of the striatal sensorimotor compartment compared with cortical representation is critical for understanding the role of the striatum in motor behavior. The first fMRI study to address the somatotopical representation of the striatum has reported a foot and hand representation in the putamen similar to that observed in non-human primates (Lehéricy et al., 1998). Since then, other reports have further extended these findings for face movements (Maillard et al., 2000
) and suggested that activation was less lateralized in the basal ganglia than in the cortex (Scholtz et al., 2000).
Several questions remain to be elucidated. Studies in primates (Künzle, 1975; Hikosaka et al., 1989
; Alexander and Crutcher, 1990
; Parthasarathy et al., 1992
; Flaherty and Graybiel, 1993
) and preliminary studies in humans (Lehéricy et al., 1998
; Maillard et al., 2000
; Scholz et al., 2000
) have suggested a dorsal to ventro-medial representation of the foot, hand and face area in the putamen, and a predominant representation of eye movements in the caudate nucleus. In humans, a comprehensive study of the three-dimensional (3-D) somatotopic representations of the foot, hand, face and eye areas is still lacking. The degree of overlap between each territory is also still debated (Lehéricy et al., 1998
; Maillard et al., 2000
). Within the putamen, the projections zones of the ipsi- and contralateral sensorimotor cortices in primates tended to interdigitate rather than completely overlap (Flaherty and Graybiel, 1993
). Basal ganglia, which are connected to bilateral cortical areas, may show more frequent bilateral activation during unilateral movements than in the primary sensorimotor cortex.
The aims of the present study were: to determine the 3-D somatotopic representation of the foot, hand, face and eye areas in the striatum; to study the degree of overlap between these territories and between the projection zones of the ipsi- and contralateral hand areas; and to study further the laterality of basal ganglia activation compared with other cortical areas.
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Materials and Methods |
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Seven right-handed, healthy volunteers were studied (six men, one woman; age range 2431 years). The French National Ethics Committee approved the study. All subjects gave informed consent. Handedness was confirmed by a test of laterality (Dellatolas et al., 1988).
Imaging
The MR protocol was carried out using at 1.5 T whole-body system using blood oxygen level dependent (BOLD) fMRI. The head of the subject was immobilized using foam cushions and tape. The protocol included: (i) one sagittal T1-weighted image to localize functional and anatomical axial slices; (ii) 20 axial gradient echo echo-planar (EPI) images (5 mm no gap, TR = 3000 ms, TE = 60 ms, bandwidth = 125 kHz, = 90°, FOV = 240 x 240 mm2, matrix size: 64 x 64, in-plane resolution = 3.75 x 3.75 mm); and (iii) 110 axial contiguous inversion recovery 3-D fast SPGR images (1.5 mm thick, TI = 400 ms, FOV = 240 x 240 mm2, matrix size = 256 x 256) for anatomical localization. Images were acquired over 6090 min.
Tasks
The subjects performed five different tasks: (i) flexion/extension of the fingers of the right hand; (ii) flexion/extension of the fingers of the left hand; (iii) flexion/extension of the toes of the right foot; (iv) contraction of the lips; and (v) saccadic eye movements. Saccadic eye movements consisted in horizontal ocular movements of 20° in the leftward and rightward directions performed in the dark with eyes closed. All movements were self-paced. Specific instructions concerning the movements to be made were given to the subjects immediately before the experiment. Movements were shown to the subjects by the experimenter at a rate of
1 Hz, without any explicit instruction given concerning the movement frequency. Before the scan, subjects performed each movement for
1530 s. The frequency at which the movement was spontaneously performed by the subject was monitored by the experimenter (
1 Hz) before and during the scan. During the scan, the subjects laid in the dark with eyes closed. In the rest condition, they were told to remain in a resting awake state. Task switching instructions were recorded on a digital audio device and presented using standard headphones customized for fMRI experiments and inserted in a noise-protecting helmet that provided isolation from scanner noise. One hundred and twenty-four EPI volumes were acquired over 6 min 12 s for each of the five different tasks. During this period, subjects alternated 15 epochs of 24 s of rest (R) and motor conditions (M): MRMRMRMRMRMRMRM). The first four volumes of each sequence were discarded to reach signal equilibrium.
Analysis
All data analyses were performed with statistical parametric mapping, v. 99 (SPM 99; Wellcome Department of Cognitive Neurology, London, UK). For each subject, anatomical images were transformed stereotactically to Talairach coordinates (Talairach and Tournoux, 1988). 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 fixed effect analysis)
For group analysis, data from each run were modeled using the general linear model with separate delayed boxcar functions modeling hemodynamic responses of each period of tasks. Overall signal differences between runs were also modeled. A temporal cut-off of 120 s was applied to filter subject-specific low frequency drift related mostly to subject biological rhythms. An SPM {F} map was obtained, reflecting significant activated voxels according to the model used (P < 0.001). Separate analyses were performed during all motor tasks. To test hypotheses about regionally specific condition effects, the estimates were compared using linear contrasts comparing motor tasks and rest. The resulting set of voxel values for each contrast constituted an SPM {T} map. The resulting set of T-values was then thresholded at P < 0.05 (T > 4.78). Data were corrected for multiple comparisons inside the volume of the whole brain. For basal ganglia, data were first thresholded at T > 3.09 (P < 0.001). In these thresholded maps, activated clusters were corrected for multiple comparisons inside the volume of the striatum [small volume correction (Worsley et al., 1996)] and considered significant if their spatial extent was >4 voxels, corresponding to a P < 0.05 corrected. In this case, the small volume correction is valid because the statistical analysis is guided by a very strong anatomical hypothesis, with well-defined and invariant anatomical landmarks across subjects (Worsley et al., 1996
). To study the degree of overlap between areas activated during the different movements in the striatum, data were analyzed as a function of the statistical thresholds (from P = 106 to P = 102) uncorrected for multiple comparison, as the degree of overlap depends on the statistical threshold used to detect activation. For individual analysis, parametric maps were constructed using the same contrasts and thresholds as for the group analysis.
Three-dimensional Anatomical Localization in the Basal Ganglia
The 3-D reconstruction of the basal ganglia was obtained using semi-automatic segmentation software based on region growing. Activation maps in the basal ganglia were superimposed on 3-D reconstructions of the normalized images. Overlap between clusters activated in the striatum during the various motor tasks was calculated using dedicated automatic software.
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Results |
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Somatotopic Representation of the Foot, Hand and Face Areas in the Putamen
In the group analysis (P < 0.05, corrected for multiple comparison), activation was contralateral to right finger movements and bilateral for foot and left hand movements (Table 1). Bilateral lip movements were associated with bilateral activation in the putamen. Saccadic eye movements were associated with activation in the anterior part of the right putamen. Within the left putamen, pixels activated during movements of the foot were located in the dorsal part of the structure, pixels activated during lips movements were located more ventrally and medially, and pixels activated during hand movements were located in between (Figs 1 and 2
). No significant pixel was activated in the left putamen during eye movements. Activation largely predominated at the level of the anterior commissure and in the post-commissural putamen (Figs 1 and 2
). Some activated pixels were also found in the pre-commissural putamen.
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For hand movement, activation was larger in the contralateral than the ipsilateral putamen. Ipsilateral activation was more prominent for the non-dominant than the dominant hand movements (Table 4). In the left putamen, ipsilateral activation tended to be anterior to contralateral activation (Fig. 4
). The activated zones of the ipsi- and contralateral hand areas were largely separated with only moderate overlap (11% of the right hand area in the left putamen at P < 0.001). In the right putamen, activation during right hand movement was weak and largely overlapped with activation during left hand movement.
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In the group analysis, the caudate nucleus was not activated during right hand and foot movements (Table 1). Bilateral activation was observed during saccadic eye movements extending from the head of the caudate into the body of the nucleus (Table 1
, Fig. 5
). Right caudate activation was also observed during left hand and lip movements (Table 1
).
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Activation was also observed in the ventral striatum during left hand and lip movements.
Signal Intensity Variation
Signal changes, expressed as the average percent, were slightly lower in the putamen (1.54, 1.89 and 1.67% during finger, lip and toe movements in the left putamen, respectively) than in the primary sensorimotor cortex (1.84, 1.88 and 1.90% during finger, lip and toe movements in the left hemisphere, respectively).
Signal changes were 1.80% in the caudate nucleus and 1.85% in the frontal eye field (FEF) during eye movements.
Thalamus
Activation was observed in the ventrolateralventral postero-lateral areas of the thalamus (comprising the somatosensory, cerebellar and pallidal afferent territories of the thalamus), contralateral to the moving hand or foot and bilaterally during lip and eye movements (Table 1).
Cortex
For hand, foot and lip movements, activation was observed in the primary sensorimotor cortex, premotor cortex, supplementary motor area, inferior frontal area (BA44/45), secondary somatosensory area (SII) and cerebellum (Table 1). In the primary sensorimotor cortex, activation was always contralateral to the moving fingers or toes (Table 3
). Bilateral activation was observed in the inferior frontal area and SII (Tables 1 and 3
). For saccadic eye movements, activation was observed in the FEF and supplementary eye field (SEF; Tables 1 and 3
).
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Discussion |
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Somatotopic Representation of Foot, Hand and Face in the Putamen
The foot area was located in the dorsal part of the structure, the face area was located more ventrally and medially, and the hand area was located in between (Figs 1 and 2). Studies in rats (Brown and Sharp, 1995
) and primates (Künzle, 1975
; Alexander and DeLong, 1985
; Liles and Updyke, 1985
; Kimura, 1990
; Flaherty and Graybiel, 1993
; Parent and Hazrati, 1995
) have shown a pronounced degree of somatotopic coding in corticostriatal projections. Anatomical studies of the somatotopic body representation in the striatum using anterograde tracers (Künzle, 1975
; Flaherty and Graybiel, 1993
) have reported a similar footdorsal, faceventromedial organization, and the arm area between the foot and the face areas. Electrophysiological studies using microstimulation and microelectrode recordings in the putamen have provided similar results (Alexander and DeLong, 1985
; Liles and Updyke, 1985
; Kimura, 1990
, 1992
). A more rostral situation of the foot area has also been described, but was not found in the present study. However, unlike the somatotopic maps of the sensorimotor cortex, striatal projections from different body parts of the primary sensorimotor cortex seem to be distributed in patches in the matrix, with a confluent dense main field and fainter satellite zones (Flaherty and Graybiel, 1993
). This pattern has been compared with the fractured somatotopy described in the cerebellum with multiple patchy representation of body parts. This raises the question of whether such an organization is specific to the squirrel monkey and related to its different locomotor behavior (Flaherty and Graybiel, 1993
), or whether it is common across species and represents a characteristic of striatal somatotopy.
In humans, the present results confirm our preliminary study at 3 T for foot and hand representation (Lehéricy et al., 1998). More recently, a triangular pattern has been reported in the putamen, with the face medial to foot and hand representation (Maillard et al., 2000
). The present study is more in favor of somatotopic pattern in vertico-oblique bands on coronal sections, with the face area more ventral and medial and the foot more dorsal and lateral (Fig. 2
), in agreement with animal studies (Alexander and Crutcher, 1990
; Brown and Sharp, 1995
). Centers of mass distances between territories tended to be higher in the present study than previously reported (Maillard et al., 2000
). The currently limited spatial resolution of fMRI studies may account for these differences between studies. Individual analysis suggested that activated areas were not distributed uniformly, but rather tended to appear as discrete zones reminiscent of the patchy distribution observed in primates. It remains to be determined whether this organization reflects the presence of a single discontinuous body map or of separate functionally differentiated body maps in the putamen (Flaherty and Graybiel, 1993
). Given the limited spatial resolution of conventional magnets compared to histological studies, this patchy distribution needs to be confirmed at higher spatial resolution. Studies at very high field strength may help elucidate this point (Yacoub et al., 2001
). Furthermore, very high field MRI may also provide information on other smaller basal ganglia nuclei, such as the pallidum, the subthalamic nucleus and the substantia nigra, which are not yet accessible to conventional magnets.
Segregation or Convergence of Sensorimotor Areas
Overlap between somatotopic territories is a matter of debate: it may be limited (Lehéricy et al., 1998) or more prominent (Maillard et al., 2000
). Overlap between distant cortical territories in the putamen may have functional significance in allowing interaction between information about different body parts. Using fMRI, the degree of overlap depends on several factors, such as the spatial resolution of functional images, data processing, which often includes image spatial filtering, field strength and the statistical threshold used to detect activation. Results in the present studies show that overlap between foot, hand and lip territories was only partial, mainly observed at the periphery of each territory. Overlap was limited between the foot and the other two territories and larger between the hand and face territories. This fits well with animal data. In monkeys, although overlap was uncommon for the dense main field of distant somatotopic zones, it was the rule for the fainter satellite zones surrounding these dense zones, even for body parts as distant as foot and hand (Flaherty and Graybiel, 1993
).
Ipsi-versus Contralateral Representation of Hand Areas in the Putamen
In contrast to the primary sensorimotor cortex, in which activation was always contralateral to the moving fingers or toes, activation in the putamen was bilateral for unilateral hand and foot movement, confirming previous reports (Scholz et al., 2000). For hand movement, activation was larger in the contralateral than the ipsilateral putamen. Although motor cortical areas project mainly to ipsilateral subcortical structures, a substantial fraction of these connections also project contralaterally via the corpus callosum (Wiesendanger et al., 1996
). In monkeys, the primary sensorimotor cortex sends a modest contralateral projection (Flaherty and Graybiel, 1993
; Wiesendanger et al., 1996
), whereas the SMA sends nearly symmetric bilateral projections (McGuire et al., 1991
; Wiesendanger et al., 1996
). Similarly, pallido-thalamic projections are known to be bilateral (Hazrati and Parent, 1991
). These bilateral projections probably represent the anatomical substrate of bilateral striatal activation. In monkeys, contra- and ipsilateral hand projections formed distinguishable input system in the putamen, largely avoiding each other (Flaherty and Graybiel, 1993
). This organization suggests that the putamen segregate motor information about the ipsilateral and contralateral distal part of the body (Flaherty and Graybiel, 1993
). The present results are consistent with animal data (Flaherty and Graybiel, 1993
), as the projection zones of the ipsi- and contralateral hand areas in the left putamen were largely separated, with only moderate overlap. However, ipsilateral activation tended to be anterior to contralateral activation, in contrast to non-human primates in which projections were at approximately the same antero-posterior levels (Flaherty and Graybiel, 1993
). This may be due to the concomitant activation of the SMA territory in the putamen, which has been located more rostrally than the primary sensorimotor territory in monkeys (Selemon and Goldman-Rakic, 1985
).
Thalamic activation was only observed in the hemisphere contralateral to the moving hand and foot. Thus, information related to unilateral limb movement may be conveyed through the basal ganglia in both hemispheres and converge to the contralateral thalamus. This point needs to be confirmed, however.
Saccadic Eye Movement and Caudate Nucleus Activation
Saccadic eye movements were associated with bilateral activation in the caudate nucleus. Caudate nucleus activation was more specifically observed during saccadic eye movements, whereas caudate activation was rarely observed during the other tasks. Caudate nucleus activation extended from the head of the caudate well into the body of the nucleus, predominating at the same coronal level of the anterior pole of the thalamus. Activation in the right putamen, also observed during saccadic eye movements, was located nearby right caudate activation (Fig. 4). These data are in agreement with non-human primate studies (Künzle and Akert, 1977
; Shook et al., 1991
; Parthasarathy et al., 1992
). Anatomical studies showed that the FEF and SEF projected principally to the caudate nucleus and adjoining parts of the putamen. Within the caudate nucleus, the projection field of these two regions was located at the coronal level of the rostral pole of the thalamus (Künzle and Akert, 1977
), or extended from the level of the anterior pole of the putamen to the posterior body of the caudate nucleus (Shook et al., 1991
; Parthasarathy et al., 1992
). In contrast to these studies, the anterior part of the caudate nucleus, which also receives SEF and FEF projections, was not activated. Electrophysiological studies in primates have suggested that neurons in more rostral parts of the caudate nucleus were activated during tasks which require higher-order processes than simple saccadic eye movements (Hikosaka et al., 1989
). In humans, a previous fMRI study has reported a predominance of caudate activation during saccadic eye movements, without further precision on the localization (Scholz et al., 2000
).
Cortico-subcortical Loop
Motor-related activation occurred mainly in the putamen at the level of the anterior commissure and in the post-commissural putamen. This area corresponds to the sensorimotor territory of the striatum in primates, the major target of cortical efferents from the primary motor and somatosensory cortices (Künzle, 1975; Alexander and DeLong, 1985
; Liles and Updyke, 1985
; Alexander and Crutcher, 1990
; Kimura, 1990
; Flaherty and Graybiel, 1993
; Brown and Sharp, 1995
; Parent and Hazrati, 1995
). In positron emission tomography (PET) and fMRI studies, Talairach coordinates of peak activation in the putamen during simple finger movements, such as a highly practiced sequence (Jenkins et al., 1994
), a repetitive movement of the middle finger (Jueptner et al., 1997
), or flexion/extension of all fingers (Lehéricy et al., 1998
), were similar to those observed in the present study. The same applies for foot movement: 27, 6, 11 (Lehéricy et al., 1998
) compared with 30, 0, 9 in the present study. Small interstudy variation may be due the limited spatial resolution of functional images and to differences in data analysis. In these tasks and in the present tasks, cortical activation was mainly restricted to the motor cortex, the posterior SMA and the cerebellum. However, when subjects learned a new sequence of finger movements with additional cognitive demand (Jenkins et al., 1994
; Jueptner et al., 1997
), generated a random sequence of finger movements making a new decision on each trial as to which finger to move (Jueptner et al., 1997
), or imagined hand movements (Gerardin et al., 2000
), more anterior parts of the striatum were activated (caudate nucleus and putamen rostral to the anterior commissure), as well as pre-frontal cortex and the anterior cingulate area. Thus, the different territories of the basal ganglia may be activated during movements in relation to specific cortical areas corresponding to the cortico-basal gangliathalamo-cortical loops described in monkeys (Alexander and Crutcher, 1990
; Parent and Hazrati, 1995
).
In summary, these results show the 3-D somatotopic organization of the human striatum, confirming the foothandface disposition along a dorsal to ventromedial gradient in the putamen. Overlap between somatotopic territories was present, although variable, depending on the level of statistical stringency. This overlap may allow interaction between information about different body parts. Comparison between the projection zones of the ipsi- and contralateral hand areas in the left putamen suggested that they were not identical, as described in primate studies. Saccadic eye movements were more specifically associated with caudate nucleus activation, in line with animal studies.
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Footnotes |
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