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An Event-Related Functional MRI Study Proc. Natl. Acad. Sci. USA Vol. 96, pp. 8301–8306, July 1999 Psychology Right hemispheric dominance of inhibitory control: An event-related functional MRI study H. GARAVAN*, T. J. ROSS, AND E. A. STEIN Department of Psychiatry, Medical College of Wisconsin, Milwaukee, WI 53226 Edited by Marcus J. Raichle, Washington University School of Medicine, St. Louis, MO, and approved May 11, 1999 (received for review February 22, 1999) ABSTRACT Normal human behavior and cognition are to target probability, whereas anterior cingulate activation also reliant on a person’s ability to inhibit inappropriate thoughts, discriminated subjects with high and low false-alarm rates (8). impulses, and actions. The temporal and spatial advantages of The distributed network thought to underlie response inhibi- event-related functional MRI (fMRI) were exploited to iden- tion, as observed with neuroimaging studies, includes the tify cortical regions that showed a transient change in fMRI supplementary motor area (SMA) (9–11), dorsal and ventral signal after the withholding of a prepotent motor response. frontal regions (7, 10–13), anterior cingulate (8, 11, 14, 15), The temporal specificity of the event-related fMRI design also and the occipital and parietal lobes (9, 14, 16). minimized possible contamination from response inhibition This widespread activation is somewhat at odds with the errors (i. e., commission errors) and other extraneous pro- animal lesion literature, which typically ascribes response cesses. Regions identified were strongly lateralized to the right inhibition to predominantly ventral frontal regions (16, 17). hemisphere and included the middle and inferior frontal gyri, One hypothesis to reconcile these observations is that the frontal limbic area, anterior insula, and inferior parietal lobe. additional regions detected in human neuroimaging experi- Contrary to the prominence traditionally given to ventral ments may not actually be necessary for response inhibition but frontal regions for response inhibition, the results suggest may reflect additional cognitive processes recruited when that response inhibition is accomplished by a distributed performing inhibition tasks. This hypothesis may be especially cortical network. germane when task activation is averaged over blocks of trials that may include both response errors and post-error processes The ability to suppress irrelevant or interfering stimuli or in which subjects may engage. Alternatively, response inhibi- impulses is a fundamental executive function essential for tion may be subserved by a network of cortical areas, of which normal thinking processes and, ultimately, for successful living. the ventral frontal region may be a necessary but not sufficient Response-inhibition deficits have been implicated in such component. To determine whether response inhibition is clinical syndromes as attention deficit hyperactivity disorder indeed mediated by more than inferior frontal regions, we (1), Tourette’s syndrome (2), obsessive-compulsive disorders exploited the temporal (and cognitive) specificity afforded by (3), and assorted ‘‘disinhibition syndromes’’ (4). The ability to event-related functional MRI (ER–fMRI). selectively attend to a subset of a complex environment, ER–fMRI. To maintain response prepotency, a mixing of activate appropriate meanings during verbal and written lan- frequent responses and infrequent response inhibitions is guage comprehension, and activate appropriate memories at ideal. The ER–fMRI design allows response inhibitions to be encoding and retrieval may all be critically dependent on the distributed throughout the testing session rather than grouped ability to suppress interfering stimuli, interpretations, and together, as in a block design. The desirable characteristic that memories, respectively (5). Onset of inhibitory abilities, as response inhibition should be effortful can result in significant indexed by the A-not-B task, also marks an important mile- numbers of errors of commission. Including these errors in a stone in cognitive development and is considered a character- block design adds both unwanted variance to the response istic of frontal lobe maturation (6). Understanding the neu- inhibition condition and unknown post-error processes, as roanatomical bases of inhibitory control, knowledge that could subjects are typically aware when they have committed errors. be used to understand its development and its contribution to This contamination may be especially problematic if one is normal cognitive functioning or pathological disruption, pro- comparing populations that differ in performance (18). Block vided the impetus for the present study. designs may also require separate stimulus and response Neuroanatomical Basis of Inhibitory Control. Typically, controls for cognitive subtraction (14, 18). Most advanta- inhibition in a laboratory setting is operationalized as the geously, the ER–fMRI design allows one to exclude errors suppression of a prepotent response. By using such an ap- from the functional analyses, thereby isolating activation as- proach, activity in ventral prefrontal cortices has been shown sociated solely with correct response inhibitions. to be modulated by manipulating the probability of nontargets, thereby affecting response-inhibition demands (7). Activation METHODS in ventral prefrontal regions has also been shown to separate Task. Fourteen right-handed subjects (6 female; mean age, subjects with high false-alarm rates from those with low Ϯ false-alarm rates on a discrimination task (8). However, con- 31 8; range: 19–44) gave informed consent and participated sistent with the distributed activations that underlie most in this study, which was approved by the institutional review cognitive processes, neuroimaging studies have revealed cere- board of the Medical College of Wisconsin. Subjects were bral activation beyond ventral frontal regions during response presented with a stream of letters presented serially every 500 inhibition. To substantiate this point, Casey and colleagues (7) msec with 0-msec interstimulus interval. Subjects made a observed that dorsolateral prefrontal regions were responsive button response whenever certain target letters (X or Y) were The publication costs of this article were defrayed in part by page charge This paper was submitted directly (Track II) to the Proceedings office. Abbreviations: fMRI, functional MRI; ER–fMRI, event-related payment. This article must therefore be hereby marked ‘‘advertisement’’ in fMRI; SMA, supplementary motor area. accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. e-mail: hgaravan@ PNAS is available online at www.pnas.org. mcw.edu. 8301 Downloaded by guest on September 30, 2021 8302 Psychology: Garavan et al. Proc. Natl. Acad. Sci. USA 96 (1999) presented. An additional rule stipulated that responses must alternate between the targets, such that if the most recent target was, for example, the letter X, then subjects should only respond to the next letter Y in the letter stream (see task schematic in Fig. 1). Consequently, subjects would have to inhibit responding if the next target letter was an X. These nonresponse targets (lures) were presented on average every 20 sec and valid targets every 3.5 sec. A minimum of 15 sec (30 letters) separated consecutive lures. Prepotency to respond to the targets was established by prior training that contained few lures (two runs of 250 letters each with 75 targets and no lures, followed by one run of 250 letters with 38 targets and 7 lures). During the scanning session, response prepotency was maintained by including six times more valid targets than lures and through prior instructions that stressed fast responding (subjects were encouraged to respond to a target while it was still on screen, that is, within 500 msec). Subjects completed four runs with 250 letters per FIG. 2. ER–fMRI time-series analysis. Example of an average run. In total, there were 150 targets and 25 lures. fMRI time series, time-locked to correct response inhibitions, taken fMRI Parameters. Contiguous 7-mm sagittal slices covering from a voxel in the dorsolateral prefrontal cortex of one subject. The ␥ the entire brain were collected by using a blipped gradient- averaged data are represented by ■ and the best-fitting -variate echo, echo-planar pulse sequence (TE ϭ 40 msec; TR ϭ 2,000 function is represented by the smooth line. The portion of the curve ϭ ϫ ϫ before departure from baseline was fitted with a flat line. Departure msec; FOV 24 cm; 64 64 matrix; 3.75 mm 3.75 mm points were constrained to occur within 4 sec of the lure presentation. in-plane resolution). All scanning was conducted on a 1.5T GE The scaling parameter, k, was free to vary, whereas the exponential Signa scanner equipped with a 30.5 cm internal diameter parameters were constrained as follows: 8 Յ r Յ 9, 0.15 Յ b Յ 0.45. three-axis local gradient coil and an endcapped quadrature To provide a measure of the response magnitude, the area under the birdcage radio frequency head coil (19). High-resolution curve was expressed as a percentage of the area under the baseline, spoiled gradient recalled acquisition at steady state (GRASS) determined by the linear portion of the fitted model and its contin- anatomic images were acquired before functional imaging to uation (shown as a dashed line). allow subsequent anatomical localization of functional activa- voxel time series while retaining a hemodynamic waveform. tion.
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