Cognitive and Behavioral Correlates
Rosemary Tannock, Ph.D.


NIH Consensus Development Conference
on Diagnosis and Treatment
of Attention Deficit Hyperactivity Disorder

November 16–18, 1998
National Institutes of Health

The following is an abstract of the presentation of Rosemary Tannock, Ph.D. on cognitive and behavioral correlates to AD/HD. The abstract is designed for the use of panelists and participants in the conference and as a reference document for anyone interested in the conference deliberations. We are grateful to the author for summarizing her materials and making them available in a timely fashion.
(Graphics and tables version available for easier reading)
Cognitive and Behavioral Correlates
Rosemary Tannock, Ph.D.

Neuropsychological correlates provide useful criteria for examining the validity of attention deficit hyperactivity disorder (ADHD), because they do not share method variance with clinical measures used to assess psychiatric symptomatology. Performance is assessed directly and is not subject to confounding factors such as recall bias or halo effects. Also, these data provide insights into the neural substrates of the disorder (Halperin, McKay, 1998; Lezak, 1995).

A systematic review of the literature was undertaken using Medline and Psychlit bibliography databases and covering the following correlates: (1) general intellectual function, (2) academic achievement, (3) neuropsychological function (motor function, perception, visual-motor integration, language, memory, executive functions), and (4) cognitive processes (alerting, orienting, executive control). The following questions were addressed: (1) What are the impairments/strengths associated with ADHD? (2) Do these impairments/strengths vary by gender and/or by age? (3) Are these impairments/strengths influenced by the presence of concurrent disorders? (4) Are these impairments/strengths specific to ADHD? and (5) What neural networks are implicated?

General Intellectual Function

Intelligence tests provide a broad index of higher cortical functioning that can be used to generate hypotheses for further investigation using neuropsychological and experimental cognitive techniques. Their psychometric properties remain robust for the clinical group of ADHD (Schwean, Saklofske, 1998). Compared with normative data, ADHD is associated typically with lower full-scale IQ and subtest scores (particularly those comprising an index of working memory), but the mean levels of intellectual functioning are well within the normal range. These findings are robust across age (preschool through adulthood), gender (although girls may exhibit greater intellectual impairment), study design (cross-sectional, longitudinal) or source of sample (epidemiological, pediatric, or psychiatric clinic), and various test versions (Saklofske, Schwean, Yackalic, et al., 1994; Sonuga-Barke, Lamparelli, Stevenson, et al., 1994; Mariani, Barkley, 1997; McGee, Williams, Moffit, et al., 1989; Barkley, DuPaul, McMurray, 1990; Biederman, Faraone, Taylor, et al., 1998; Seidman, Biederman, Faraone, et al., 1997; Seidman, Biederman, Faraone, et al., 1997; Gaub, Carlson, 1997). Also, they generally hold for studies that have controlled for the presence of comorbid disorders (Faraone, Biederman, Lehman, et al.,1993; Faraone, Biederman, Weber, et al., 1998; Newby, Recht, Caldwell, et al., 1993). By contrast, the findings do not appear to hold for the predominantly hyperactive subtype of ADHD, suggesting that the intellectual profile may be a correlate of inattention rather than hyperactivity/impulsiveness (Gaub, Carlson, 1997; Semrud-Clikeman, Biederman, Sprich, et al., 1992; Hinshaw, 1992; Barkley, Anastopoulos, Guevremont, et al., 1991). Preliminary evidence that male (but not female) siblings of children with ADHD exhibit a similar intellectual profile supports the hypothesis that ADHD is familial (Faraone, Biederman, Lehman, et al., 1993). This intellectual profile is not specific to ADHD; it is also associated with learning disabilities and other disruptive behavior disorders (Newby, Recht, Caldwell, et al., 1993). Thus, intellectual correlates of ADHD may have conceptual but not diagnostic significance.

Academic Achievement

Academic achievement tests provide a more detailed profile of strengths and weaknesses in underlying component skills that contribute to academic competency and indicate the presence of a learning disability. One of the most robust findings is a higher rate of school failure (Semrud-Clikeman, Biederman, Sprich, et al., 1992; Hinshaw, 1992; Barkley, Anastopoulos, Guevremont, et al., 1991). This is evidenced most clearly by low productivity but also by lower scores (on average, 0.5 S.D. lower) on reading (decoding, comprehension), spelling, and arithmetic, and elevated rates of grade repetition, learning disabilities, remedial tutoring, and special class placement, despite average levels of intellectual functioning. Academic underachievement is evident in both girls and boys as well as siblings, it occurs in preschool years and endures through adolescence (Barkley, DuPaul, McMurray, 1990; Faraone, Biederman, Lehman, et al., 1993; Faraone, Biederman, Weber, et al., 1998; Zentall, 1990). It is a correlate of ADHD per se and cannot be accounted for by psychiatric comorbidity (which tends to influence school placement rather than school failure or intellectual ability) or comorbid learning disabilities (Faraone, Biederman, Lehman, et al., 1993; Faraone, Biederman, Weber, et al., 1998). However, academic problems, particularly in arithmetic, are more common among predominantly inattentive and combined subtypes of ADHD, suggesting that these problems are related to inattention rather than hyperactivity/impulsivity (Hynd, Lorys, Semrud-Clikeman, et al., 1991; Baumgaertel, Wolraich, Dietrich, 1995; Lahey, Applegate, McBurnett, et al., 1994; Gaub, Carlson, 1997; Lamminm @ ki, Ahonen, N @ rhi, et al., 1995; Marshall, Hynd, Handwerk, et al., 1997. The nature of the academic impairments (particularly in individuals without comorbid learning disabilities) suggests problems in effortful processing. However, there is no evidence of a profile that is uniquely associated with ADHD.

Neuropsychological Function

Neuropsychological tests provide a detailed assessment of a wide array of cognitive functions that afford insights into brain-behavior relationships; they are sensitive to subtle deficits that interfere with learning and achievement. The most consistent (albeit not invariable) findings are impairments in “executive functions,” an umbrella term denoting a range of higher order, effortful, self-regulatory functions whose formal definition and measurement (particularly in children) remain elusive and under debate (Pennington, 1997; Tannock, 1998; Pennington, Ozonoff, 1996). However, impairments in component functions, particularly those associated with control of motor responses (planning, inhibition) and working memory, are clearly evident during effortful tasks in preschoolers, children, and adolescents, using a variety of measures requiring both fast or slow processing of information (Mariani, Barkley, 1997; Seidman, Biederman, Faraone, et al., 1997; Seidman, Biederman, Faraone, et al., 1997; Pennington, Ozonoff, 1996; Nigg, Hinshaw, Carte, et al., in press; Seidman, Biederman, Faraone, et al.,1995). These findings generally hold after controlling for comorbid psychiatric disorders and learning disabilities (Nigg, Hinshaw, Carte, et al., in press; Seidman, Biederman, Faraone, et al., 1995). Motor planning and inhibition problems are not typically associated with learning disabilities, although a combination of impairments in motor control, perception, speech-language, and attention is discernible in some children (Gillberg, Rasmussen, Carlstrom, et al., 1982; Hellgren, Gillberg, Bagenholm, et al., 1994). Reciprocally, verbal impairments associated with reading disabilities (phonological processing, verbal memory) are not associated with ADHD (Javorsky, 1996; Felton, Wood, 1989). Moreover, verbal impairments reflecting difficulties in use of language for organization of information and self-regulation (language-mediated processing) are more strongly associated with ADHD than with learning disabilities (Tannock, Schachar, 1996). These patterns of findings indicate at least some neuropsychological differentiation between these overlapping disorders. On the other hand, evidence of impairments in many component functions (including motor inhibition) in a wide range of clinical populations mitigates specificity for ADHD (Gold, Carpenter, Randolph, et al., 1997; Matier-Sharma, Perachio, Newcorn, 1995; Purcell, Maruff, Hyrios, et al., 1998).

Information Processing

Methods derived from information processing theory allow decomposition and more precise measurement (latency and accuracy) of the complex web of cognitive processes involved in most neuropsychological measures (Cohen, 1993). The most robust finding is of slow, variable, and inaccurate response latencies across a range of different measures, implicating impairments in energetic state regulation, preparation, maintenance, and inhibition or adjustment of motor control processes. Three component processing systems are implicated: sustained attention or vigilance, which refers to a state of readiness to respond (CPT paradigms) (Losier, McGrath, Klein, 1996; Corkum, Seigel, 1993; Van der Meere, 1996; Sergeant, Van der Meere, 1990), selective attention or spatial allocation of attention (visuospatial orienting paradigms) (Nigg, Swanson, Hinshaw, 1997; Pearson, Yaffee, Loveland, et al., 1995; Swanson, Posner, Potkin, et al., 1991; Tannock, Schachar, Logan, 1993), and response inhibition (stop-signal, delay-aversion paradigms) (Sonuga-Barke, Taylor, Hepenstall, 1992; Sonuga-Barke, Williams, Hall, et al., 1996; Oosterlaan, Logan, Sergeant, 1998; Schachar, Logan, 1990; Schachar, Tannock, Marriott, et al., 1995). The findings are not incontrovertible. For example, impairments in sustained attention are evident across the lifespan (preschool through adulthood) regardless of comorbidity, but findings are influenced strongly by temporal parameters (interstimulus interval, trial length, etc.), stimulus modality, memory load, and context (presence/absence of experimenter, rewards) (Purcell, Maruff, Hyrios, et al., 1998; Cohen, 1993; Van der Meere, 1996; Sergeant, Van der Meere, 1990; Halperin, Wolf, Greenblatt, et al., 1991b; Chee, Logan, Schachar, et al., 1989). In general, ADHD is associated with inefficient performance (slow, inaccurate) and vigilance decrements (faster than normal decline in performance) that occur with increased demand for effortful processing (Van der Meere, 1996; Sergeant, Van der Meere, 1990). However, performance impairments on vigilance tasks are exhibited by a wide range of clinical populations, once again challenging the notion of specificity for ADHD per se. Dysfunction of the visuospatial orienting system (particularly in the right hemisphere) is suggested by a few studies of covert orienting (shifts in allocation of visual attention in the absence of saccadic eye movements), including one study of biological parents, suggesting the influence of genetic factors (Nigg, Swanson, Hinshaw, 1997; Pearson, Yaffee, Loveland, et al., 1995; Swanson, Posner, Potkin, 1991). However, inconsistency of findings across studies and across child and parent samples does not allow for firm conclusions.

Response inhibition deficits are demonstrated using theoretically distinct methods. One approach characterizes the impairment as delay avoidance, defined as a response style aimed at minimizing total time on task (Sonuga-Barke, Taylor, Hepenstall, 1992; Sonuga-Barke, Williams, Hall, et al., 1996). The continuity of this response style into adulthood or its variation with gender or comorbidity is unknown. Another approach demonstrates impairments in inhibiting prepotent courses of action (indexed by slow and/or variable inhibitory processes) (Oosterlaan, Logan, Sergeant, 1998; Schachar, Logan, 1990; Schachar, Tannock, Marriott, et al., 1995). The severity of impairment is attenuated in the situational and predominantly inattentive subtypes (suggesting a closer association with hyperactivity/impulsivity), as well as by comorbid anxiety (Schachar, Logan, 1990; Schachar, Tannock, Marriott, et al., 1995). These inhibition deficits are shared by other externalizing disorders (aggression, oppositional defiant disorder, conduct disorder) but are not evident in anxiety disorders or learning disabilities, suggesting some specificity with hyperactivity/impulsivity (Oosterlaan, Logan, Sergeant, 1998). Moreover, there is preliminary evidence of a link between performance decrements on response inhibition tasks and subtle anatomical anomalies in the frontal-striatal circuitry (prefrontal cortex, caudate, and globus pallidus) in children and adolescents with ADHD (Casey, Castellanos, Giedd, 1997). It is not known whether these deficits continue into adulthood, and there is little evidence that this central inhibitory control impairment relates to behavioral self-regulation (impulsivity, overactivity, inattention).


Implications for Neural Substrate and Pathophysiology of ADHD

The pattern of neuropsychological impairments associated with ADHD shows correspondence with findings of subtle anomalies in brain anatomy and neurochemistry in individuals with ADHD (Tannock, 1998). Specifically, vigilance deficits implicate neural networks in the right frontal lobe and locus ceruleus; impairments in response control and cognitively demanding information processing implicate the dopaminergically mediated “anterior” attentional system associated with anterior cingulate and frontostriatal circuitry; and the potential deficits in visuospatial orienting implicate “posterior” attentional systems comprising superior parietal cortex, pulvinar, and superior colliculus (Posner, Raichle, 1994). Moreover, the overall difficulties in dynamic, online adjustment and adaptation to changes in the immediate environment, which are evident in both clinical and cognitive studies of ADHD, implicate cerebellar networks that play a major integrative role in prediction and preparation of neural conditions needed for a particular motor or nonmotor operation (Courchesne, Allen, 1997).


Future Directions

Currently, ADHD is best characterized as reflecting a nonoptimal activation state and dysfunction in motor preparation and control (planning, execution, inhibition) not readily explainable by comorbidity, but not necessarily specific to ADHD. This research is challenged by heterogeneity of this symptom complex, measurement problems, and the study of small samples. Future studies may be more informative if ADHD is conceptualized as a composite of two quantitative, continuously distributed dimensions of inattention and impulsivity/ hyperactivity, rather than as three categorical subtypes. Also, large samples are required to afford adequate statistical power for multivariate techniques to examine the impact of gender, age, symptom dimensions, and comorbidity. Comparisons with multiple clinical/medical groups are required to examine the issue of specificity of neuropsychological impairment. Measurement approaches are required that select measures of contrasting constructs (automatic versus controlled processing, linguistic versus non-linguistic, fast versus slow pace, motoric versus nonmotoric, high versus low working memory load, etc.) and incorporate the recent advances in brain imaging and psychophysiological techniques. Delineation of the neuropsychological and neural mechanisms of ADHD must be an iterative process in which clinical subtypes are defined, tested, and redefined, using more precisely controlled and validated measures.



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