Characterizing cognition in ADHD: beyond executive dysfunction

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The hypothesis that Attention-Deficit/Hyperactivity Disorder (ADHD) reflects a primary inhibitory executive function deficit has spurred a substantial literature. However, empirical findings and methodological issues challenge the etiologic primacy of inhibitory and executive deficits in ADHD. Based on accumulating evidence of increased intra-individual variability in ADHD, we reconsider executive dysfunction in light of distinctions between ‘hot’ and ‘cool’ executive function measures. We propose an integrative model that incorporates new neuroanatomical findings and emphasizes the interactions between parallel processing pathways as potential loci for dysfunction. Such a reconceptualization provides a means to transcend the limits of current models of executive dysfunction in ADHD and suggests a plan for future research on cognition grounded in neurophysiological and developmental considerations.

Introduction

Attention-deficit/hyperactivity disorder (ADHD) is characterized by pervasive behavioral symptoms of hyperactivity, impulsivity and inattention, beginning in childhood [1]. Despite its high prevalence and associated lifelong impairment [2], ADHD remains controversial because of the use of psychostimulants for treatment of a ‘behavioral condition’ that is diagnosed subjectively [3]. The heritability of ADHD is, however, both substantial and solidly established. Although major risk genes have yet to be identified, several genes related to monoaminergic neuromodulation are confirmed as minor contributors to the overall phenotypic variance [4]. Moreover, there is robust evidence of structural, functional and neurochemical brain differences in ADHD, in regions that support vital cognitive functions [5]. Thus, a coherent and comprehensive model of the cognitive substrates of ADHD would be a highly desirable means of linking genetic, neurobiological and phenotypic levels of analysis, with the objective of improving diagnostic approaches and therapeutic options.

Such a model should eventually encompass ADHD throughout the lifespan. However, the ADHD literature is preponderantly based on children of elementary school age. As neuropsychological differences are most detectible at this age [6], this brief review will generally exclude studies on preschool-age-children or adults, despite remarkable consistency between cognitive deficits across these wide age ranges. We defer attempts to synthesize initial efforts at linking cognitive and neuronal phenotypes to current candidate genes, all of which have minor effects at best [4]. Similarly, active areas of potentially related research, such as psychopharmacology [7] or neuroimaging 8, 9, which have been recently reviewed elsewhere, are not covered, but will certainly contribute to fully integrated models. Our purposes here are to reassess currently dominant cognitive models of ADHD in light of empirical and conceptual challenges and to highlight an integrative model that incorporates emerging neuroanatomical perspectives. We believe that this approach will provide a more robust framework for the translational multidisciplinary efforts that are already underway in laboratories throughout the world.

Section snippets

Evolving cognitive models of ADHD

The explicit criteria for ADHD that were first codified in 1980 (see historical review in [10]) emphasized inattention as much as hyperactivity, based on robust objective evidence of behavioral inattention and performance deficits on a laboratory measure of attention, the continuous performance task [11]. However, when specific attentional processes were targeted (i.e. divided, selective, sustained), investigators failed to observe specific diagnostic deficits [12]. Based on parallels between

Cognitive heterogeneity of ADHD: multiple pathway models

The cognitive literature is thus incompatible with the assumption of pathophysiological homogeneity – of a single core deficit. Researchers have responded by building models that accept heterogeneity 41, 44, 45 – in which ADHD is regarded as an umbrella construct with clinical value that subsumes multiple potentially dissociable but overlapping cognitive profiles. So far, too few studies include measures from different functional domains (EF, reinforcement/motivational, sensory/perceptual and

‘Hot’ and ‘cool’ executive functions

In considering potential synthetic linkages between EF and processes related to motivation such as underlie Delay Aversion, a line of work on the development of EF is particularly pertinent. Noting the functional differentiations within frontal cortices, Zelazo and Muller distinguish between more purely cognitive aspects of EF associated with dorsolateral prefrontal cortex (DLPFC) which are characterized as ‘cool’ as contrasted with relatively ‘hot’ affective aspects of EF associated with

Conclusion

The EF/inhibition model of ADHD set the stage for an impending paradigm shift in the neuropsychology of ADHD. ADHD is undeniably associated with ‘cool’ EF deficits at a group level of analysis, but the predicted central role of inhibitory and executive deficits is not supported for a substantial proportion of children with ADHD. ‘Hot’ EF deficits have been examined less frequently and yet may be more relevant from the perspective of functional outcomes and real-world decision making.

Acknowledgements

The authors appreciate the assistance of Daniel Margulies in preparing the manuscript, Suzanne Haber for providing the figure, and Phil Zelazo for helpful comments on an earlier version. Supported by grants to F.X.C. from NIMH (MH066393), The Stavros S. Niarchos Foundation, NARSAD, and the Leon Lowenstein Foundation, Inc.

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