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Differential Activation of Dorsal Basal Ganglia During Externally and Self

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Differential Activation of Dorsal Basal Ganglia During Externally and Self Brain Imaging 1111 Website publication 21 April 1998 NeuroReport 9, 1567–1573 (1998) 2 3 THEbasal ganglia are thought to be critically involved 4 in motor control. However, the relative contributions of Differential activation 5 the various sub-components are not known. Although, 6 in principle, functional magnetic resonance imaging of dorsal basal ganglia 7 (fMRI) provides adequate resolution to image the basal during externally and 8 ganglia at the spatial scale of the individual nuclei, acti- vating these nuclei with fMRI has proven to be difficult. 9 Here we report two tasks, involving externally and self self paced sequences 10111 paced sequences of arm movements, which resulted in 1 significant activation of contralateral posterior (post- of arm movements 2 commissural) putamen and globus pallidus. This activa- 3 tion did not significantly differ between the tasks. In V. Menon,1,3,CA G. H. Glover2 contrast, significant activation of the contralateral and 1,4 4 ipsilateral anterior caudate and anterior putamen was and A. Pfefferbaum 5 observed only during externally paced arm movements. 6 These results suggest a dissociation in the roles of the Departments of 1Psychiatry and Behavioral 7 anterior and posterior dorsal basal ganglia: the anterior Sciences and 2Radiology, Stanford University 8 caudate and putamen may be involved in sensory to School of Medicine, Stanford, CA 94305-5550; motor mapping and the posterior putamen and globus 9 3Palo Alto VA Health Care System; and pallidus may be involved in the motor response itself. 4 20111 The findings support the hypothesis that the basal SRI International, USA 1 ganglia may be involved in gating sensory influences 2 onto motor areas . NeuroRepor t9: 1567–1573 © 1998 3 Rapid Science Ltd. 4 Key word s: Basal ganglia; Caudate; fMRI; Globus pallidus; 5 Motor control; Motor sequencing; Putamen; Striatum CACorresponding Author 6 7 8 9 30111 1 Introduction nucleus.4–6 Thus, for example, Deiber et a l .6 found 2 no differences in left lentiform nucleus activation 3 The dorsal striatum and globus pallidus are thought when directions of joy stick movements were cued 4 to play an important role in movement initiation, by the pitch of tones, freely selected or always in a 5 control and sequencing.1 Thus, for example, patients forward direction. Reviewing these and a number of 6 with Parkinson’s disease, which is characterized by other studies has led Brooks7 to comment that the 7 depletion of striatal dopamine, have difficulty with role played by the basal ganglia in controlling motor 8 self-initiated or volitional movements.2 A potentially function remains enigmatic. 9 powerful approach to investigating the motor func- One reason for this negative finding might be 40111 tion of the dorsal basal ganglia has been to examine that PET studies do not have the effective spatial 1 differences between self and externally paced move- resolution to distinguish between sub-regions of the 2 ments. Romo et a l .3 examined the anterior striatum basal ganglia nuclei. Functional magnetic resonance 3 in monkeys performing self-initiated and stimulus- imaging (fMRI) provides greater spatial resolution 4 triggered arm reaching movements and found a segre- that PET and, in principle, could provide the spatial 5 gated population of neurons engaged in internally resolution to differentiate between sub-components 6 generated movements. More importantly, they of the basal ganglia. However, attempts to activate 7 also report that more neurons were active during the putamen and globus pallidus in our and other 8 externally triggered movements. On a larger spatial laboratories with complex finger movements have not 9 scale, several positron emission tomography (PET) been successful. One fMRI study reported activation 50111 studies have examined lentiform nucleus (putamen while subjects performed pronation and supination 1 and globus pallidus) activation during motor tasks hand movements.8 However, this task is not partic- 2 that involved self-initiated or self-paced and exter- ularly amenable to manipulations in the cognitive, 3 nally triggered movements in neurologically normal perceptual or motor dimensions. 4 subjects. These studies found differences in activa- The aim of this report is twofold. First, and most 5 tion in the dorsolateral prefrontal cortex and the importantly, to demonstrate fMRI activation of the 6111p supplementary motor area but not in the lentiform dorsal basal ganglia during two sequencing tasks, one © Rapid Science Ltd Vol9No7 11 May 1998 1567 V. Menon, G. H. Glover and A. Pfefferbaum 1111 involving externally paced arm movements and the microprocessor (http://poppy.psy.cmu.edu/psyscope) 2 other involving self paced arm movements. We connected to the Macintosh. Audio signals were 3 hypothesized that the higher motor load involved in amplified using a home audio receiver, transmitted to 4 making arm (as opposed to finger) movements would a piezo-electric speaker placed near the head of the 5 result in detectable activation of a region of interest scanner and then piped binaurally to the subjects. 6 (RoI) that included the dorsal striatum and globus 7 pallidus. Second, to describe the differential activa- Acquisition: Images were acquired on a conven- 8 tion of sub-regions of the RoI during these tasks and tional 1.5T GE (Milwaukee, WI) scanner using a 9 discuss its implications for dorsal basal ganglia func- quadrature whole head coil. Subjects lay with their 10111 tion. Both multisubject and single subject data were head restrained using a bitebar.10 Twelve axial slices 1 analyzed. (6 mm thick, 0 mm skip), extending roughly from –10 2 to 62 mm relative to the anterior commissure, were 3 imaged with a temporal resolution of 4 s at 120 time 4 Materials and Methods points using a T2* weighted gradient echo spiral pulse 5 sequence (TR = 1000 ms, TE = 40 ms, flip angle = 6 Subjects: Twenty-two healthy right-handed sub- 40°, 4 interleaves).11 Field of view was 310 mm and 7 jects (aged 20–35 years) participated in the study after the effective inplane spatial resolution was 4.35 mm. 8 giving written informed consent. Eleven subjects (six Images were reconstructed, by inverse Fourier trans- 9 men and five women) performed the externally paced form, for each of the 120 time points into 256 ´ 256 20111 arm movement task while 11 other subjects (seven ´ 12 image matrices (resolution: 1.21 ´ 1.21 ´ 6 mm). 1 men and four women) performed the self-paced are Images corresponding to the first two time points 2 movement task. The two groups did not differ signif- were discarded from further analysis to eliminate 3 icantly in gender (p > 0.5; Fisher’s exact test). non-equilibrium effects. 4 High resolution whole brain images were also 5 Experimental design: The tasks consisted of 12 acquired to localize activation foci, using a T1- 6 alternating 40 s epochs of rest and arm movements. weighted spoiled grass gradient recalled (SPGR) 3D 7 Subjects rested the closed fist of their right hand on MRI sequence: (TR = 24 ms; TE = 4 ms; flip angle = 8 the base of a palm-shaped keypad. Movement 40°; 24 cm field of view; 124 slices in sagittal plane; 9 consisted of touching, with thumb and forefinger 256 ´ 192 matrix; acquired resolution = 1.5 ´ 0.9 ´ 1.2 30111 pinched together, the tip of one of four ‘fingers’ mm) reconstructed as a 124 ´ 256 matrix (resolution: 1 15 cm away from the base. Subjects were explicitly 1.5 ´ 0.9 ´ 0.9 mm). 2 instructed to avoid finger movement. Subjects 3 practised the task briefly for 2 min and 40 s (four Preprocessing: fMRI data were pre–processed using 4 epochs) 30 min before the scan and were monitored SPM96 (http://www.fil.ion.bpmf.ac.uk/spm). Images 5 visually during the scan to verify consistent task were corrected for movement using least square mini- 6 performance. mization without higher-order corrections for spin 7 In the externally paced arm movement task, history. Images were normalized to stereotoxic 8 numbers between 1 and 4 were presented with an Talairach coordinates and resampled every 2 mm 9 ISI of 2 s. Subjects in this group made arm move- using sinc interpolation. 40111 ment to corresponding locations on the keypad after 1 each number. In the self-paced arm movements task Region of interest: The region of interest (RoI) 2 group, subjects first mentally generated three consisted of the dorsal striatum and globus pallidus 3 numbers between 1 and 4 and then made arm move- in both hemispheres. In addition to all of the 4 ments to corresponding locations on the keypad, putamen, the dorsal striatum also included the 5 returning to base after each number and repeating portion of the caudate anterior to the anterior 6 this with a new sequence until 40 s elapsed and commissure, i.e. in the caudate head. Since each 7 they were verbally instructed to ‘STOP’. After a subject’s brain was normalized to Talairach space, 8 40 s rest period they were told to ‘BEGIN’. Pilot voxels in the RoI were defined on a Talairach 9 data had indicated that generating three numbers at template image. The number of voxels in the RoI in 50111 a time roughly balanced the number of movements Talairach space was 3008. 1 between the two tasks. 2 The task was programmed using Psyscope9 on a Statistical analysis: Individual voxels activated by 3 Macintosh (Sunnyvale, CA) notebook computer. the tasks was identified using regression analysis as 4 Initiation of scan and task was synchronized implemented in SPM96.12–14 A reference waveform 5 using a TTL pulse delivered to the scanner timing consisting of +1 for motor task images and –1 for 6111p microprocessor board from a CMU Button Box rest images was used to predict the main effect of 1568 Vol 9 No 7 11 May 1998 Differential activation of dorsal basal ganglia 1111 task.
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