Covert visual spatial attention in boys with attention deficit hyperactivity disorder: Lateral effects, methylphenidate response and results for parents
Introduction
Childhood attention deficit hyperactivity disorder (ADHD) is common and impairing, but the nature of the attention deficit remains a neuropsychological puzzle [40]. ADHD is diagnosed behaviorally from persistent, age-inappropriate inattention, impulsivity and overactivity [2]. These behavior problems lead to family, peer and achievement difficulties and place such children at long-term risk for poor social and achievement outcomes [20]. Etiology of ADHD is not well understood, but possible neuropsychological or neurobiological deficits remain important in current theories.
Current neurobiological theories agree on the importance of frontal cortex (especially orbitofrontal, premotor and prefrontal areas) and subcortical (especially striatal, i.e. caudate, putamen) structures 4, 16, 17, 23, 45. Intriguing, but less agreed-upon, is possible hemispheric asymmetry of attentional dysfunction in ADHD. Some neurocognitive theories do not feature asymmetry (e.g. [4]). Others suggest hemispheric asymmetry in ADHD, but differ regarding the nature of the asymmetry 17, 22, 23, 42. One proposal emphasizes primarily right-sided frontal–striatal abnormalities [17]. A related but different formulation emphasizes bilateral frontal–striatal dysfunction, in which interhemispheric regulation of catecholamine systems is disrupted 23, 24. Both frontal and striatal structures are important to the deployment of visual spatial attention [10]. Therefore, if the asymmetry theories are correct, ADHD should be associated with lateral abnormalities (e.g. subclinical neglect) in attention allocation. Many researchers have contributed, but for convenience we refer to the Heilman et al. [17]and the Malone et al. [23]theories.
All neurobiological theories of ADHD emphasize brain catecholamine function, in large part because of the established clinical response to stimulant medication of children with ADHD 17, 23, 24, 45. The theories also predict asymmetric brain hemisphere response to stimulant medications (e.g. methylphenidate, the most commonly used pharmacologic treatment for ADHD). Brain catecholamines also contribute to orienting of attention [7], so if these theories are correct, spatial attention might reflect the conjectured asymmetry as well.
Robertson [33]reviews approaches to assessing attention in psychopathology research. Unique advantages in assessing lateral asymmetry and subclinical neglect are attained by examining ‘covert’ visual spatial orienting. Covert orienting refers to the direction of spatial attention apart from actual eye movement [29], overcoming the confound of immature oculomotor development in children [5]. A distributed neural network model of spatial attention 10, 29contrasts warned and unwarned targets and features examination of within-subject lateral differences, and so is well-suited to evaluating hemispheric asymmetry hypotheses.
Although introduced to the field some 25 years ago, covert orienting has only recently garnered renewed interest from developmental researchers (for reviews see Refs [5]and [25]). Like adults, unimpaired youngsters exhibit equal reaction times to targets in the left visual field (LVF) and right visual field (RVF), and show normal cuing responses 11, 12, 39, although developmental changes in cuing effects have been noted 5, 25. Thus, covert orienting may afford a useful window for assessing lateral differences in attention function in child ADHD.
Covert orienting in childhood ADHD has been examined previously in two published reports of which we are aware 25, 39. Although both studies found abnormalities in ADHD, only the latter examined lateral asymmetry [39]. We chose the widely-used, non-invasive cue–target detection paradigm developed by Posner 27, 28, 39for our study. In this task, subjects fix attention at a central point on a computer display and press a button in response to targets appearing in either visual field. A cue (luminosity change) precedes the appearance of the target on most trials, and on most trials is on the same side as the target (a valid cue). In a minority of trials, however, the cue is contralateral to the target (an invalid cue). In normal adult and child subjects, the valid cue orients attention to the target's presentation and speeds reaction time, whereas the invalid cue orients attention away from the target's presentation and slows reaction time 5, 39. The no-cue condition taps reactivity to new stimuli. The contrast between valid and invalid cue conditions, termed the Validity Effect, is an index of the system's capacity to prepare for an anticipated target. Further, when the cue–target interval (or stimulus–onset asynchrony) is less than about 350 msec for children [5]and about 150 msec for adults [28], the subject does not have time for an eye movement—thus only ‘covert’ or automatic, early stage attention processing is thought to be involved. With longer intervals motor movement (e.g. eye saccade) may influence responses 5, 40. No response choice is required for this simple detection task; the subject merely presses a key in response to the target. Accuracy is high, and reaction time is the usual dependent measure.
The prior study of ADHD with this paradigm [39]featured two cue–target delays, one at 100 msec and the other at 800 msec. The 100 msec delay condition allows assessment of orienting and alerting prior to eye movement; the 800 msec condition allows assessment of how well attention to a target location is maintained. ADHD but not comparison children had slower reaction times to RVF than LVF targets, in both the no cue and invalid cue conditions, but only when the cue–target delay was 800 msec. ADHD children also displayed a larger Validity Effect in the RVF than in the LVF. Stimulant medication equalized the lateral response times.
We conducted three studies designed to advance research on covert orienting in ADHD. In Study 1 we attempted to replicate the prior findings [39]and to evaluate several hypotheses regarding lateral abnormalities in spatial attention processing in ADHD. We confined the study to boys because of suggestions that similarly impaired boys and girls may respond differently on the orienting task 11, 39. In Study 2, we investigated the dose–response effects of a catecholamine agonist (methylphenidate, a stimulant commonly prescribed as treatment for ADHD) on visual–spatial orienting for boys with ADHD. In the third study, considering the issue of heritability in ADHD, we assessed biological and adoptive parents of ADHD youngsters.
Section snippets
Study 1
The first study examined boys with ADHD and a comparison group of non-ADHD boys. The hypotheses were based on two of the more detailed theoretical conjectures of neuropsychological function in ADHD, represented by Heilman et al. [17]and Malone et al. [23]. First, both theories suggest bilateral slower responses in the ADHD than the non-ADHD group across all conditions 17, 23. (For Heilman et al. this is because right hemisphere attentional impairment compromises attention functioning
Study 2
Study 2 comprised examination of dose–response patterns to methylphenidate (a stimulant) in the covert orienting task. The design allowed within-subject comparison of dose response in the two visual fields. Hypotheses were again based on the two representative theories of catecholamine dysfunction in ADHD.
First, based on Heilman et al.'s model, we predicted that medication would equalize responses to targets in the no-cue condition—requiring that the right hemisphere speed up more than the left
Study 3
Two questions motivated Study 3: (a) Is the different pattern of covert orienting of the ADHD and comparison groups also present in the two groups of parents, and (b) is an abnormal response pattern on this task a candidate familial marker of ADHD? Family studies can provide one means of validating putative neuropsychological markers for psychopathology categories [13].
A genetic component to ADHD has been supported 13, 38but the precise nature of the heritable contribution to ADHD remains
General discussion
These three studies support the suggestion of hemispheric asymmetry of covert spatial attention processing in ADHD, but do not clearly favor one theory of asymmetry. Two major findings, bilateral slowing in all conditions in the ADHD boys and slow reaction times to uncued LVF targets in the ADHD boys and their biological parents, imply a right-sided hemispheric dysfunction as predicted by both of the neurobiological asymmetry theories that informed the study 17, 24. Taken together, however, the
Conclusion
Despite the limitations noted, the replication of lateral asymmetry in the ADHD group, replication of asymmetrical medication response in ADHD children, and new experimental findings with parents suggest that further examination of hemispheric asymmetry in visual spatial orienting of attention in ADHD is worthwhile. Findings provide partial support for theories of ADHD that include hemispheric asymmetry of attention function. The findings suggest that theories of ADHD should distinguish
Unlinked reference
[35]
Acknowledgements
Primary work on this investigation was supported by National Institute of Health Research Service Award fellowship F31 MH10462-01 to Joel T. Nigg, and National Institute of Mental Health Grant RO1 MH45064 to Stephen P. Hinshaw. The authors wish to acknowledge the helpful comments of Richard Ivry, Michael Posner, Joseph Sergeant, and the anonymous reviewers on earlier versions of this article. We thank Gina Condon for assistance with data management and Geoff Keppel for consultation regarding
References (45)
- et al.
Catecholamines and the covert orienting of attention in humans
Neuropsychologia
(1989) - et al.
Lateralized deficits in visual attention in males with developmental dopamine depeletion
Neuropsychologia
(1992) - et al.
Neuropharmacology of methylphenidate and a neural substrate for childhood hyperactivity
Psychiatric Clinics of North America
(1985) - et al.
Long-term outcome of hyperactive children: A review
Journal of the American Academy of Child and Adolescent Psychiatry
(1991) - Achenbach, T. M. and Edelbrock, C. S. Manual for the Child Behavior Checklist and Revised Child Behavior Profile....
- American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 3rd edn, Revised. American...
- et al.
Mother–child interactions in ADHD and comparison boys: Relationships with overt and covert externalizing behavior
Journal of Abnormal Child Psychology
(1994) - Barkley, R. A. Impaired delayed responding: A unified theory of attention-deficit hyperactivity disorder. In Disruptive...
- Brodeur, D. A. Covert orienting in young children. In The Development of Attention: Research, Theory, and Practice, J....
- Cantwell, D. P. and Carlson, G. A. Stimulants. In Pediatric Psychopharmacology: The Use of Behavior Modifying Drugs in...