NIH Consensus Development Conference
on Diagnosis and Treatment
of Attention Deficit Hyperactivity Disorder
November 1618, 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.
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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 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 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).
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,
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).
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
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