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Article Parietal Attentional System Aberrations During Target Detection in Adolescents With Attention Deficit Hyperactivity Disorder: Event-Related fMRI Evidence Leanne Tamm, Ph.D. Objective: Directed attention, the ability Results: Individuals with ADHD made to allocate and direct attention toward a significantly more errors of commission Vinod Menon, Ph.D. salient stimulus, is impaired in attention than comparison subjects. Further, rela- deficit hyperactivity disorder (ADHD). This tive to comparison subjects, individuals Allan L. Reiss, M.D. construct is often assessed with target de- with ADHD showed significantly less acti- tection or oddball tasks, and individuals vation in the bilateral parietal lobes (in- with ADHD perform poorly on such tasks. cluding the superior parietal gyrus and However, to date, the specific brain struc- supramarginal and angular gyri of the in- tures or neural mechanisms underlying ferior parietal lobe), right precuneus, and thalamus. target detection dysfunction in individu- als with ADHD have not been identified. Conclusions: Adolescents with ADHD The authors’ goal was to investigate neu- demonstrated significant impairments in ral correlates of target detection dysfunc- their ability to direct and allocate atten- tion in ADHD using event-related fMRI. tional resources. These difficulties were associated with significant aberrations in Method: Behavioral and brain activation the parietal attentional system, which is data were collected while subjects per- known to play a significant role in atten- formed a visual oddball task. Participants tion shifting and detecting specific or sa- included 14 right-handed male adoles- lient targets. Thus, dysfunction in the pa- cents with ADHD (combined type) and 12 rietal attentional system may play a typically developing age- and handed- significant role in the behavioral pheno- ness-matched male comparison subjects. type of ADHD. (Am J Psychiatry 2006; 163:1033–1043) Attention deficit hyperactivity disorder (ADHD) is a ADHD commit more errors of commission (failure to behavioral disorder characterized by marked problems withhold a response to frequent or standard stimuli) and with inattention, impulsivity, and hyperactivity that often have slower or more variable reaction times than causes significant functional impairment in multiple set- comparison subjects (4, 5). Further, individuals with tings (e.g., school and home). Although behavioral and ADHD show aberrant event-related potentials (i.e., de- cognitive deficits in ADHD are well described, there is little creased P300 latency and amplitude) in response to odd- consensus regarding the specific brain structures or neu- ball or rare target stimuli in conjunction with poorer be- ral mechanisms underlying dysfunction in individuals havioral performance relative to comparison subjects (4– with this disorder (1). To further elucidate this issue, a va- 8). Thus, it appears that impairments in directed attention riety of laboratory paradigms have been used, including are characteristic of ADHD. A clearer understanding of the tasks involving target detection and response inhibition. underlying neural correlates of these deficits in ADHD will One such paradigm is the “oddball task,” which involves be important in diagnosis and treatment planning. detection and response to infrequent (oddball) target Although event-related potential studies index the tim- events embedded in a series of repetitive events. Following initial sensory processing, target detection involves the ing and sequence of neuronal activity underlying cogni- process of bringing a salient stimulus into conscious tive processes, this technique is limited because of poor awareness for further evaluation, categorization, and re- spatial resolution (i.e., a number of current distributions sponse. This task is thought to capture the construct of di- in the brain can give rise to identical field distributions on rected attention and reflects an individual’s ability to the scalp [2]). Thus, complementary methods are needed monitor the environment for change and decide on a to determine the neural correlates of target detection. In course of action, a critical survival skill (2, 3). particular, the advent of noninvasive functional MRI Studies that have investigated target detection or odd- (fMRI) has allowed investigation of the neural correlates of ball task performance have reported that individuals with such functions as target detection, thus contributing to a Am J Psychiatry 163:6, June 2006 ajp.psychiatryonline.org 1033 NEURAL CORRELATES IN ADHD better understanding of executive dysfunction observed group reported current use of stimulant medication; all five were in neuropsychiatric disorders such as ADHD. subjected to an 18-hour washout of their stimulant medication To date, there have been no fMRI studies investigating prior to the scan. In addition, all participants did not have caf- feine at least 2 hours before the scan, and of those reporting drug target detection or oddball task performance in an ADHD use (two in the ADHD group, one in the comparison group) and population. However, five fMRI studies have investigated alcohol use (three in the ADHD group, six in the comparison response inhibition in ADHD populations using go/no go group), a 3-week washout period for drugs (typically marijuana) type tasks and block (9–11) and event-related designs (12, and a 1-week washout period for alcohol were observed. 13). The go/no go and oddball tasks are somewhat like Typically developing comparison subjects were screened (via telephone interview with their primary caretaker and a follow-up mirror images of one another, with go/no go type tasks in- written questionnaire) for absence of neurological, developmen- volving response inhibition in the context of frequent re- tal, and psychiatric disorders and no family history of specific sponse generation, and oddball tasks involving response psychiatric disorders (i.e., ADHD, bipolar disorder, substance generation in the context of frequent response inhibition abuse/dependence, and conduct disorder/antisocial personality (14). It is unclear whether response inhibition (the act of disorder). All individuals in the comparison group scored in the normative range (<65) on the Child Behavior Checklist (25). withholding or suppressing a response) differs from that ADHD diagnosis was determined through a structured clinical of selecting an alternative response. interview conducted with the primary caregiver of each partici- To examine these processes and associated dysfunction pant during the initial telephone screening and was verified dur- in ADHD, we designed two event-related fMRI tasks, a go/ ing the initial visit (Diagnostic Interview for Children and Adoles- no go task controlling for novelty (13) and an oddball task. cents–Version IV [DICA-IV] completed by primary caregiver). In addition, each primary caregiver completed the Conner ADHD/ In this study, we used a standard visual-based oddball task DSM-IV scale–Parent Version about their adolescent (ADHD In- similar to that used in other fMRI studies (15), with a mod- dex Score: mean=75.5, SD=10.0). Individuals with a family history ification that controls for motor responding. This type of of bipolar disorder were excluded from participation. One partic- task also has been referred to as a “change task” (16) or a ipant in the ADHD group met diagnostic criteria for current ma- response selection task (14). Individuals with ADHD are jor depression and was excluded from analyses to avoid con- founds related to psychomotor retardation. known to perform poorly on these tasks (16). To familiarize subjects with the MRI environment and to mini- We predicted that individuals with ADHD would make mize artifacts related to movement, a protocol using an MRI sim- more errors of commission than typically developing ulator was administered to subjects in the ADHD group. Specifi- healthy comparison subjects on the oddball task. Al- cally, a movie viewed by the subject during the simulated scan though no previous fMRI studies have investigated odd- would cutoff for 3 seconds whenever the subject moved beyond a set criterion. Increasingly stringent movement criteria (decreas- ball task performance in ADHD subjects, previous fMRI ing from 3 to 1 mm) and increasing time periods (2 minutes, 5 studies of normal subject performance on oddball para- minutes, 10 minutes) were selected until all subjects met a crite- digms have reported activation to target stimuli in the in- rion of less than three movements exceeding 1 mm within a 10- ferior and middle frontal gyri (15, 17–19) as well as tempo- minute period. Exclusion criteria of head movement greater than ° ral regions (superior temporal gyrus [Brodmann’s area 22] 3 mm and rotation less than 3 during fMRI scanning were estab- lished; no participants exceeded this movement threshold. and middle temporal gyrus) and parietal regions (inferior Cognitive functioning was assessed with the Wechsler Abbrevi- parietal lobules [including supramarginal gyrus] and su- ated Intelligence Scale (WAIS), and academic functioning (i.e., perior parietal lobe) (2, 15, 17–20). On the basis of mor- reading, spelling, and arithmetic) was assessed with the Wide phological studies (21) and functional imaging studies of Range Achievement Test, Third Edition (WRAT-III). response inhibition (9–13) implicating these regions in Experimental Task ADHD, we predicted that activation might be aberrant in In the event-related oddball task, stimuli