Adaptive control deficits in attention-deficit/hyperactivity disorder (ADHD): The role of error processing
Introduction
Children with attention-deficit hyperactivity disorder (ADHD) are characterized as being distractible and disorganized. Adaptive goal-directed behavior requires the constant comparison of ongoing actions with internal goals and standards. If discrepancies between expected and actual outcomes are being detected, adaptive control processes are called into play in order to make behavioral adjustments. Adaptive control processes are critical in novel situations, when multiple tasks need to be managed at the same time, or when information in the environment threatens to trigger an inappropriate action, situations in which patients with ADHD are typically impaired. Therefore, a deficit in high-level control processes, labelled “executive control" has been proposed (Barkley, 1997a, Douglas, 1999, Sergeant, 2000, Berger and Posner, 2000, Nigg et al., 2004). More specifically, it has been suggested that ADHD children fail to use performance errors and inappropriate response tendencies to determine whether control processes need to be tightened (Barkley, 1997b, Douglas, 1999, Sergeant, 2000). This inability leads to a deficit in flexibly regulating task performance as reflected by high error rates and variable response latencies (Sergeant, 1988, Leth-Steensen et al., 2000, Kuntsi et al., 2001, Castellanos and Tannock, 2002). Evidence for an inefficient utilization of errors to adjust performance comes from studies assessing the degree of response slowing after subjects have committed an error in speeded reaction time tasks. While normal children shift towards a more conservative speed/accuracy balance following an error, ADHD children do not use such a strategy to prevent future errors (Sergeant and van der Meere, 1988, Krusch et al., 1996, Schachar et al., 2004). It remains to be clarified why children with ADHD fail to implement appropriate control adjustment.
Since the discovery of the error-related negativity (ERN), considerable progress has been made in studying how the brain determines and communicates the need to recruit control. The ERN is a sharp negative deflection in the event-related potential (ERP) with a fronto-central distribution, which peaks approximately 80 ms after an incorrect response (Falkenstein et al., 1991, Gehring et al., 1993). Source localization studies have demonstrated that the ERN has a medial–frontal generator, most likely the anterior cingulate cortex (ACC; Dehaene et al., 1994). According to early theories, the ERN reflects a mismatch between intention and action (Gehring et al., 1993), or, alternatively, the simultaneous activation of two competing responses (Carter et al., 1998). A recent theory holds that when an error has been made, a fast alert and teaching signal, indicating unexpected absence of reward is carried via midbrain dopamine (DA) neurons from the basal ganglia to the ACC (Holroyd and Coles, 2002). Very recently, it has been proposed that the ACC detects conditions under which errors are likely to occur rather than errors or conflict itself (Brown and Braver, 2005). Modulation of activity in the ACC (related to monitoring) serves as a signal that engages control processes in lateral pre-frontal cortex (PFC) and, as a consequence, leads to changes in performance (Ridderinkhof et al., 2004) since stronger behavioral adjustment on the next trial is associated with increased lateral PFC activity (Garavan et al., 2002, Kerns et al., 2004).
A growing body of literature suggests that cognitive control deficits in ADHD arise from a dysfunction in a DA-rich fronto-striatal network of brain structures, including the ACC, since functional abnormalities have been reported during various effortful tasks that engage cognitive control (Lou et al., 1989, Vaidya et al., 1998, Rubia et al., 1999, Bush et al., 1999, Ernst et al., 2003, Durston et al., 2003, Fallgatter et al., 2004, Tamm et al., 2004, Schulz et al., 2004, Booth et al., 2005). The ERN has been shown to be altered in pathological conditions associated with fronto-striatal DA dysfunction, such as Parkinson's disease (Falkenstein et al., 2001), obsessive–compulsive disorder (Gehring et al., 2000), and Tourette's syndrome (Johannes et al., 2002).
In the present study, we employed a modified version of the Eriksen flanker Paradigm (Eriksen and Eriksen, 1974), a task frequently used in ERN research. The flanker task measures the ability to suppress inappropriate response tendencies elicited by irrelevant information. In order to further increase the likelihood of committing an error, the task was performed under time pressure. Response time variability and runs of errors and correct responses were calculated to determine the frequency and magnitude of performance fluctuations. Furthermore, using the ERN as a psychophysiological index of error detection, and post-error slowing as a measure of behavioral adjustment following an error, we investigated whether deficient error processing may underlie ADHD children's poor adaptive control.
Section snippets
Participants
Sixteen boys, aged 8 to 12 years (M = 128.5 months, S.D. = 15.4) with a clinical diagnosis of ADHD were recruited via advertisement on a website on the internet where they could sign up for participation in the study. Children with comorbid developmental disorders including learning difficulties and dyslexia, Tourette's syndrome, epilepsy and pervasive developmental disorder were excluded. Additional exclusion criteria included auditory or visual problems and medication other than methylphenidate.
Overall performance
As a result of the response deadline manipulation, all children responded faster when time pressure was high (626 ms) as opposed to low (765 ms), and committed more errors under high time pressure (15.0%) than under low time pressure (7.9%). In addition, they responded slower and committed more errors when conflict elicited by distracting arrows was high as opposed to low (congruent trials: 8.5%, 644 ms, respectively; incongruent trials: 14.4%, 747 ms, respectively), indicating that our
Discussion
The present findings demonstrate that a disruption in the brain's error checking system may underlie a failure to implement adequate cognitive control in children with ADHD performing a speeded choice reaction task. Although their performance was not compromised in terms of response speed and regularity, ADHD children failed to achieve the same level of accuracy as control children, particularly when confronted with time pressure and response conflict, as indicated by increased error rates.
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2019, International Journal of Psychophysiology