Introduction raphy PET or functional magnetic resonance imaging

Brain Research 879 2000 204–215 www.elsevier.com locate bres Interactive report Laterality, somatotopy and reproducibility of the basal ganglia and 1 motor cortex during motor tasks a,c b a a a a Verena H. Scholz , A.W. Flaherty , E. Kraft , J.R. Keltner , K.K. Kwong , Y.I. Chen , a a , B.R. Rosen , B.G. Jenkins a MGH-NMR Center , Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02119, USA b Department of Neurology , Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02119, USA c Department of Diagnostic Radiology , Klinikum Grobhadern, Ludwig-Maximilians-University, Munich, Germany Accepted 1 August 2000 Abstract We investigated the basal ganglia, motor cortex area 4, and supplementary motor area SMA using functional magnetic resonance imaging fMRI and five motor tasks: switching between finger and toe movements, writing, finger tapping, pronation supination, and saccadic eye movements. We found reliable activation in the caudate nucleus and putamen in single subjects without the need for inter-subject averaging. Percent signal changes in basal ganglia were smaller by a factor of three than those in SMA or motor cortex 1 vs. 2.5–3. There was a definite foot-dorsal, hand-ventral basal ganglia somatotopy, similar to prior data from primates. Saccadic eye movements activated the caudate nucleus significantly more than the other tasks did. Unilateral movements produced bilateral activation in the striatum even when motor cortex activation was unilateral. Surprisingly, bilateral performance of the tasks led, on average, to consistently smaller basal ganglia activation than did unilateral performance P,0.001, suggesting less inhibition of contralateral movements during bilateral tasks. Moreover, there was a striking dominance pattern in basal ganglia motor activation: the left basal ganglia were more active than the right for right handers, regardless of the hand used. This lateralization appears much stronger than that previously reported for motor cortex. Comparisons of inter-subject and intra-subject reproducibility indicated a much larger variability in basal ganglia and SMA compared to motor cortex, in spite of similar percent signal changes in the latter two structures.  2000 Elsevier Science B.V. All rights reserved. Theme : Motor systems and sensorimotor integration Topic : Basal ganglia Keywords : Functional magnetic resonance imaging; Striatum; Putamen; Motor control; Laterality; Extrapyramidal system; Inhibition

1. Introduction raphy PET or functional magnetic resonance imaging

fMRI have become robust tools for identifying brain In spite of much study on the functional role of the basal areas related to motor behavior in humans and can depict ganglia, their specific role in motor control remains activity in the lentiform putamen, globus pallidus and unknown [2,3]. Anatomical and electrophysiological de- caudate nucleus. fMRI, with its excellent spatial resolution, scription of the individual nuclei are relatively well is a powerful technique to further study the role of these established, especially in animals, but it is not as easy to subregions of the basal ganglia in motor control describe their multistage interactions during motor control. However, there are some even simpler, important, Neuro imaging techniques as positron emission tomog- questions related to organization of basal ganglia activity that have not been addressed so far [20,22]. First, is there hemispheric dominance in motor activation of the len- 1 Published on the World Wide Web on 28 August 2000. tiform and caudate nucleus? In human motor cortex there Corresponding author. Tel.: 11-617-726-5816; fax: 11-617-736- is evidence for left hemispheric dominance in right-handed 7422. E-mail address : bgjnmr.mgh.harvard.edu B.G. Jenkins. subjects [17] and animal and human studies show basal 0006-8993 00 – see front matter  2000 Elsevier Science B.V. All rights reserved. P I I : S 0 0 0 6 - 8 9 9 3 0 0 0 2 7 4 9 - 9 V .H. Scholz et al. Brain Research 879 2000 204 –215 205 ganglia asymmetry [4,11,12,18]. Secondly, to what extent resolution T1-weighted images were acquired for ana- is motor control in these areas bilaterally organized? Thus, tomical location. Flow-sensitive sequences were taken as we wished to determine the degree of activation seen in the well to highlight the vessels, so that the statistical maps lentiform and caudate nucleus comparing the same tasks could be compared with the vessel images. To minimize performed both bilaterally and unilaterally. Lastly, we motion artifacts, the subjects lay supine with their head wished to ask whether the somatotopic organization of the secured by a pillow, foam wedges, and a restraining strap. input zone of the basal ganglia putamen and caudate can be mapped using current techniques and spatial resolution. 2.3. Tasks Although these areas of the basal ganglia have been somatotopically mapped in non-human primates [7,10,19] Except in the saccadic eye movement task which was it has not been done in humans. necessarily bilateral, subjects were studied using their We have chosen to investigate a series of simple motor right side, their left side, and both sides. We used a block tasks. We deliberately chose motor tasks with little cogni- design in which 6–8 blocks of 30 s of activation alternated tive component, in order to separate out as best as possible with 30 s of rest described above. In addition, 40–60 s of the motor components of the questions above. In addition, baseline images were collected. Between 16 and 42 blocks we chose to investigate five different tasks, rather than of each task were performed. In each imaging session not exhaustively study one task, to assess whether issues more than five different studies were performed, to limit related to laterality and dominance are general across an fatigue and head movement during the fMRI measure- array of motor tasks. ments. The following tasks were performed:

2. Materials and methods