A Functional MRI Study of the Human Prefrontal Cortex During A
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Proc. Natl. Acad. Sci. USA Vol. 94, pp. 6989–6994, June 1997 Neurobiology “Willed action”: A functional MRI study of the human prefrontal cortex during a sensorimotor task (positron emission tomographyyhuman brain mappingydorsolateral prefrontal cortexyverbal fluencyyBrodmann areas 6, 8, 9, 24, 32, 45, and 46) FAHMEED HYDER†‡,ELIZABETH A. PHELPS§,CHRISTOPHER J. WIGGINS¶,KEVIN S. LABAR§,ANDREW M. BLAMIREi, AND ROBERT G. SHULMAN† Departments of †Molecular Biophysics and Biochemistry and §Psychology, Yale University, New Haven, CT 06510; ¶Max-Planck-Institut fu¨r neurologische Forschung, Inselstrasse 22–26, 04103 Leipzig, Germany; and iMedical Research Council, John Radcliffe Hospital, Headington, Oxford OX3 9DU, United Kingdom Contributed by Robert G. Shulman, April 14, 1997 ABSTRACT Functional MRI (fMRI) was used to examine correct response. The difference between these two conditions human brain activity within the dorsolateral prefrontal cortex was defined as the ‘‘willed action’’ response. It was hypothe- during a sensorimotor task that had been proposed to require sized by Frith and co-workers that any common areas of selection between several responses, a cognitive concept cerebral activation found in the two cognitive tasks would be termed ‘‘willed action’’ in a positron emission tomography the result of a ‘‘willed action’’ component, because these two (PET) study by Frith et al. [Frith, C. D., Friston, K., Liddle, tasks had very few other common characteristics. In both P. F. & Frackowiak, R. S. J. (1991) Proc. R. Soc. London Ser. cognitive tasks activation in a large area of the dorsolateral B 244, 241–246]. We repeated their sensorimotor task, in prefrontal cortex was observed, which led Frith and co- which the subject chooses to move either of two fingers after workers to conclude that brain activity in this area is due to a stimulus, by fMRI experiments in a 2.1-T imaging spec- ‘‘willed action’’ and is independent of the stimulus modality trometer. Echo-planar images were acquired from four coro- (i.e., verbal or sensorimotor). However, they reported some nal slices in the prefrontal cortex from nine healthy subjects. differences in the hemispheric locations of the dorsolateral Slices were 5 mm thick, centers separated by 7 mm, with prefrontal cortex activations for the two cognitive tasks. Most nominal in-plane spatial resolution of 9.6 3 5.0 mm2 for mean significantly, brain activity for the verbal fluency task was data. Our mean results are in agreement with the PET results lateralized to the left hemisphere, whereas the activity for the in that we saw similar bilateral activations. The present results sensorimotor task was bilateral. Although the coordinates of are compared with our previously published fMRI study of a the reported center of mass (COM) of the large area of verbal fluency task, which had also been proposed by Frith et activation in the left dorsolateral prefrontal cortex differed al. to elicit a ‘‘willed action’’ response. We find a clear slightly between the cognitive tasks, being slightly superior for separation of activation foci in the left dorsolateral prefrontal the sensorimotor task, Frith et al. proposed that ‘‘willed acts in cortex for the sensorimotor (Brodmann area 46) and verbal the two response modalities studied (speaking a word, or lifting fluency (Brodmann area 45) tasks. Hence, assigning a par- a finger) were associated with increased blood flow in the ticular activated region to ‘‘willed action’’ is not supported by dorsolateral prefrontal cortex (Brodmann area 46)’’ (4). These the fMRI data when examined closely because identical differences raise the question as to whether the areas activated regions are not activated with different modalities. Similar by these two different modalities are the same, or whether modality linked activations can be observed in the original there are spatial distinctions dependent on the modality of PET study but the greater resolution of the fMRI data makes presentation or other task-specific differences. the modality linkages more definite. In the present study, we attempt to address the question of whether these two different ‘‘willed action’’ tasks produce In humans, a wide range of behavior has been attributed to the identical areas of activation. Recently, work within this labo- prefrontal cortex, including working memory (1, 2), planning and ratory has examined the verbal fluency task by using functional execution (3), willed action (4), self-awareness (5), and verb MRI (fMRI) (9). Coordinates of the activated foci in our generation (6, 7). Many other experiments have tried to differ- verbal fluency fMRI study and the COM of activations re- entiate the specific regions within the prefrontal cortex whose ported using PET (4) agreed to within the combined experi- activity is related to these varied behaviors (8). In a recent study, mental accuracy. To determine if we find similar activations Frith and co-workers (4) utilized positron emission tomography for the other ‘‘willed action’’ task, here we have performed an (PET) to localize area(s) of the prefrontal cortex involved in fMRI study during the sensorimotor task. First, we compare ‘‘willed action,’’ a cognitive concept which they identified as being the areas of activation observed in this study to the previous involved in any task that requires the subject to choose between PET findings of the same sensorimotor task (4). For this more than one equally appropriate response. purpose it was sufficient to acquire data only from the pre- In an attempt to localize prefrontal cortex activity related to frontal cortex. Second, we compare the fMRI activations ‘‘willed action,’’ Frith and co-workers (4) compared two observed in the sensorimotor task to localized activations from cognitive tasks involving different modalities: a verbal fluency our previously reported fMRI verbal fluency study (9). Finally, task and a sensorimotor task. For both tasks, they compared we compare and contrast the localized activities observed by two conditions: a baseline condition where the correct re- both methods during the verbal fluency task (4, 9, 10) and the sponse was determined by the stimulus, and a generate con- sensorimotor task (refs. 4 and 11 and the present study), to dition where the subject had to choose from more than one Abbreviations: fMRI, functional MRI; PET, positron emission to- The publication costs of this article were defrayed in part by page charge mography; EPI, echo-planar imaging; ROI, region of interest; COM, center of mass. payment. This article must therefore be hereby marked ‘‘advertisement’’ in ‡To whom reprint requests should be addressed at: 126 MRC, 330 accordance with 18 U.S.C. §1734 solely to indicate this fact. Cedar Street, Yale University, New Haven, CT 06510. e-mail: hyder@ © 1997 by The National Academy of Sciences 0027-8424y97y946989-6$2.00y0 mrcbs.med.yale.edu. 6989 Downloaded by guest on September 30, 2021 6990 Neurobiology: Hyder et al. Proc. Natl. Acad. Sci. USA 94 (1997) examine the similarities andyor differences of regional activa- Data Analysis. The data analysis in this study was identical to tions for the two ‘‘willed action’’ tasks. We demonstrate that that in the previous fMRI verbal fluency study (9). Functional the revealed areas of activation in the left dorsolateral pre- images were analyzed off-line on an Silicon Graphics Indy work- frontal cortex from these two different tasks are not the same, station (Mountain View, CA) in MATLAB environment (Natick, and that these differences in localized activity are very likely MA). Movement artifacts were assessed by a COM algorithm to be modality andyor cognitive task dependent. using noninterpolated functional images. Briefly, a thresholded image was created such that intensities of all pixels outside the brain were set to zero, whereas the intensities of all pixels inside MATERIALS AND METHODS the brain were not altered. For each data set, the deviations in the Subjects. Sixteen right-handed English-speaking subjects COMs of the thresholded images (in x and z directions of a pixel) (13 males, 3 females) volunteered for this study. Approval was were plotted against time to reveal the temporal patterns of obtained from the Human Investigation Committee of Yale motion. A data set was discarded from further analysis if the University and all subjects gave informed consent. Subjects deviation in the COM for any image in a series was greater than were placed supine on a bed. The subject’s head was firmly 25% of a pixel size [i.e., 1.2 and 0.6 mm for x and z directions in positioned in a foam-rubber holder which minimized move- stereotactic space]. This criterion for movement artifact in a series ment. All six subjects involved in the previous fMRI verbal of functional images was based on the time course of image fluency study (9) were included in this study. intensity fluctuations in the resting brain (i.e., Baseline condition Experimental Design. In both conditions presented to the images where there was no stimulus-initiated movement). No subject, an individual trial consisted of a touch on either of the attempt was made to correct for physiologic fluctuations in the first two fingers of the subject’s right hand, followed by a response fMRI data (15). from the subject. The response given was a movement of either For each run consisting of 16 images per slice, the mean of the of these fingers, depending on the particular condition. There first 4 images per slice, representing basal signal (S), was sub- were two conditions: Repeat, the subject would move the same tracted from each image within the series, thus producing 16 finger as had been touched; and Random, the subject would difference images per slice and revealing task-related signal choose which finger to move and the sequence of which finger was changes (DS). The last 4 images per slice in a run were not used touched was random.