Frontal lobe functions in attention deficit disorder with and without ...

Journal of Abnormal Child Psychology, Vol. 20, No. 2, 1992

Frontal Lobe Functions in Attention Deficit Disorder With and Without Hyperactivity: A Review and Research Report R u s s e l l A. Barkley, 1,2 Gail Grodzinsky, 1 and George J. D u P a u l I

We review 22 neuropsychological studies of frontal lobe functions in children with attention deficit disorder with and without hyperactivity (ADD/+H, ADD/-H). Some measures presumed to assess frontal lobe dysfunctions were not reliably sensitive to the deficits occurring in either form of ADD. Tests of response inhibition more reliably distinguished A D D / + H from normal children. Where impairments were found on other tests between A D D and normal subjects, they were highly inconsistent across studies and seemed strongly related to age of the subjects and possibly to the version of the test employed. Other methodological differences across studies further contributed to the discrepant reports. The co-morbidity o f other disorders, such as learning disabilities (LD) and conduct problems, with A D D may be an additional confounding factor in some, though not all, of these studies. In a separate study, children with A D D / + H (n = 12) were then compared on frontal lobe tests to three other groups: A D D / - H (n = 12), L D but no A D D (n = 11), and normal children (n = 12) statistically covarying for differences in conduct problems across groups. Most measures did not distinguish among these groups. Both A D D groups made more omission errors on a Continuous PerManuscript received in final form September 9, 1991.

This research was supported by NIMH grant MH41464 and by funds from the Department of Psychiatry, University of Massachusetts Medical Center. The authors are grateful to Judy

Tessier and Ellen Mintz-Lennick for their assistance with some of the data collection and scoring. The comments of Virginia Douglas on an earlier draft of this paper are greatly appreciated. 1Departments of Psychology and Neurology, University of Massachusetts Medical Center, Worcester, Massachusetts. 2Address all correspondence, including requests for reprints, to Russell A. Barkley, Ph.D., Department of Psychiatry, University of Massachusetts Medical Center, 55 Lake Avenue North, Worcester, Massachusetts 01655. 163 0091-0627/92/0400-0163S6.50/0 9 1992 Plenum Publishing Corporation

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formance Test (CPT) than the normal group. All three clinical groups performed more poorly on the word and interference portions of the Stroop Test. Thus, while both types of ADD share some apparent similarities in deficits on a few frontal lobe tests in this study, the totality of existing findings suggests an additional problem with perceptual-motor speed and processing in the ADD/-H group. Attention deficit disorder (ADD) comprises a heterogeneous group of children believed to have developmentally inappropriate levels of inattention, impulsivity, and, in many cases, overactivity (American Psychiatric Association, 1980, 1987). These symptoms, now called attention deficit hyperactivity disorder (ADHD), have often been compared to those of frontal lobe lesions in humans and animals (Benson, 1991; Blau, 1936; Heilman, Voeller, & Nadeau, 1991; Levin, 1938; Mattes, 1980; Still, 1902). This apparent similarity in behavior between ADD children and frontally injured patients has resulted in a number of studies examining the performance of ADD children on neuropsychological tests having some sensitivity to frontal lobe injuries in adults. After reviewing the results of these studies, the findings from a smaller set of studies that have compared children with ADD with hyperactivity (ADD/+H) to those without hyperactivity (ADD/-H) on neuropsychological measures will be discussed. Such comparisons may address the issue of whether ADD/-H is actually a subtype of the same disorder as that seen in ADD/+H or is, in fact, a distinct and dissimilar disorder.

Studies Comparing ADD/+H with Normal~Clinical Control Groups Twenty-two (22) studies which have compared A D D / + H to normal or other control groups of children using frontal lobe measures are summarized in Table I. The plethora of studies of ADD/+H children that have employed the Continuous Performance Test (CPT) have been omitted, unless other frontal lobe tests were also used. The former studies are summarized elsewhere (Barkley, 1991; Douglas, 1983; Douglas & Peters, 1979) and were not expressly attempting to evaluate frontal lobe functions in these children. Nevertheless, differences between ADD/+H and normal children are frequently found on the CPT, particularly for commission errors. Only where the study used neuropsychological measures believed to assess frontal lobe functions in ADD children was it included in this table. Several methodological features of these studies require mention. The studies by Moffitt and Silva (1988) and McGee, Williams, Moffitt, and

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Table I. Studies Evaluating Frontal Lobe Deficits in A D D / + H Neuropsychological Testsa Author

Subjects

Measures

Children Using Findings

Studies comparing A D D / + H and normal control groups 1. C o h e n et al. (1972)

20 A D D / + H 20 Normal Age: 13-16 years

Stroop test

No group differences

2. Parry (1973)

24 A D D / + H 24 Normal Age: 6--13 years

WCST Porteus mazes

A D D < normal on W C S T categories and n u m b e r correct and Porteus Mazes; A D D > normal on W C S T errors, perseverative errors, and "unique" errors

3. Hopkins et al. (1979)

70 A D D / + H 42 Normal Age: 17-24 years

Stroop test

A D D > normal on

4. Chelune et al. (1986)

24 A D D / + H 24 Normal Age: 6-12 years

WCST TMT-Color Forms Progressive Fig.

5. Gorenstein et al. (1989)

21 A D D / + H t' 26 Normal Age: 8-12 years

A D D < normal: sequential WCST memory; A D D > norStroop test mal: W C S T TMT perseverative errors, Necker Cubes Stroop interference, and Sequential Memory T M T (B)

6. Shue & Douglas (1989)

24 A D D / + H 24 Normal Age: Mean 10.3 SD 1.6 years

A D D < normal on W C S T WCST categories; A D D > norT M T (A & B) mal on W C S T perseveraG o - N o - G o Test tive and Conflicting Motor Response Test nonperseverative errors, T M T part A errors and Part B errors and time, G o - N o - G o test errors, and Conflicting Motor test

7. Breen (1989)

26 A D D / + H 13 Normal Age: 6-11 years

H a n d Movements CPT

A D D < normal on Hand Movements; A D D > normal on C P T omission errors

8. Boucagnani & Jones (1989)

28 A D D / + H 28 Normal Age: 7-10 years

WCST Stroop T M T (B)

A D D < normal: W C S T categories, % correct, and Stroop No. correct; A D D > normal: W C S T perseverative response, perseverative errors, and TMT (B)

interference time and errors (p < .07) A D D < normals on W C S T categories and T M T errors; A D D > normals on W C S T perseverative errors and % correct

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Subjects

9. Loge et al. (1990)

Measures

Findings

20 ADD/+H b 20 Control Age: 6-12 years

WCST COWAT CPT Design Fluency

No group differences

10. Mariani (1990)

34 ADD/+H 30 Normal Age: 4-5 years

WCST ADD < normal on TMT (Color Forms) Hand MoveHand Movements ments; ADD > Pegboard normal on CPT Porteus Mazes commission erCPT rors

11. Grodzinsky (1990)

66 ADD/+H 64 Normal Age: 6-11 years

WCST Stroop test COWAT Rey-Osterrieth TMT (A & B) Pegboard Porteus Mazes CPT

ADD > normal on WCST No. of trials to first category and CPT commission errors; ADD < normal on Stroop interference, COWAT, Rey age, and mazes age

12. Barr et al. (1990)

13 ADD/+H 13 Normal Age: 7-12 years

Rey

ADD < normal: standard, unpaired, and organization scores

13. Fischer et al. (1990)

100 ADD/+H 60 Normal Age: 12-20 years

WCST COWAT CPT

14. Felton et al. (1987)

13 ADD/+H No RD 40 Normal 19 RD No ADD/+H 26 ADD/+H + RD Age: 8-12 years

COWAT

Both RD groups < normals; both ADD groups < normals

15. Moffitt & Silva (1988)

14 ADD/+H No Del 14 Del. No ADD 19 ADD/+H + Del 588 Normal Age: 13 years

WCST Rey-Osterrieth TMT Pegboard WISC-R Mazes

Main effects for Del < No Del groups on Rey, TMT, Pegs, and Mazes

16. McGee et al. (1989)

12 ADD/+H 13 RD 13 ADD/+H + RD 62 Normal Age: 13 years

WCST COWAT Rey-Osterrieth TMT (B Only) Pegboard WISC-R Mazes

ADD + RD < other groups on Rey-Osterrieth

ADD > normal on CPT omission and commission errors Studies comparing ADD/+H and clinical control groups

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Author

Subjects

Measures

Findings

17. Douglas & 30 A D D / + H Benezra (1990) 24 R D 30 Normal Age: 7-12 years

Rey-Osterrieth

A D D < normal

18. Matson & Fischer (1991)

12 Externalizers 12 Internalizers 12 Normals Age: 5-12 years

WCST

Externalizers < internalizers and normal: categories; externalizers > interanlizers and normal: perseverative errors

19. McBurnett et al. (1991)

13 A D D / + H Agg 13 A D D / + H No Agg 13 No A D D / + H Agg 13 No A D D / + H No Agg Age: 5-12 years

WCST

20. Carlson et al. (1986)

20 A D D / + H 15 A D D / - H 16 Normal Age: 7-11 years

Stroop test

No differences on Stroop errors but both A D D groups > normal on time to complete test

21. T r o m m e r et aL 28 A D D / + H (1991) 13 A D D / - H 32 Control

G o - N o - G o test

A D D s > controls on total errors; ADD/+H > A D D / - H and controls on omission errors; A D D / - H > A D D / + H on early trial commission errors

22. J o h n s o n (1991) 27 A D D / + H b 33 A D D / - H Age: 11-17 years

WCST TMT Hooper test

ADD/+H < ADD/H on W C S T perseverative responses and T M T part B time

A D D / + H < no A D D / + H : % correct, categories, and conceptual responses; A D D / + H > no A D D / + H : perseverative errors Studies comparing A D D / + H and A D D / - H groups

aNote: A D D / + H = attention deficit disorder with hyperactivity or attention deficit hyperactivity disorder; R D = reading-disabled; Del = delinquent; A g g = aggression; W C S T = Wisconsin Card Sort Test; Stroop test = Stroop Color-Word Association Test; C O W A T = Controlled Oral Word Association Test; Rey-Osterrieth = Rey-Osterrieth Complex Figure Test; T M T = Trail Making Test (Parts A and B); Pegboard = Grooved Pegboard Test; C P T = Continuous Performance Test; Progressive Fig. = Progressive Figures Test; Hooper test = H o o p e r Test of Visual Organization; W l S C - R = Weschsler Intelligence Scale for Children-Revised. bThese papers did not use clinic-referred children as A D D subjects but instead used school children identified as deviant on teacher ratings.

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Anderson (1989) used the same sample of subjects from the Dunnedin longitudinal study at their 13-year-old assessment point. They differ only in their method of sorting the subjects into different co-morbid groupings, one focusing on delinquency, the other on reading disorders (RD). Similarly, the studies by Cohen, Weiss, and Minde (1972) and Hopkins, Perlman, Hechtman, and Weiss (1979) drew their subjects from the same sample of hyperactive children during a followup study, with Cohen et al. (1972) assessing them as adolescents while Hopkins et al. (1979) assessed a larger sample as adults. All studies reviewed varied greatly in their method of defining subjects as ADD/+H. All but one used specifically hyperactive or A D D / + H children, the exception being the study by Matson and Fischer (in press) which used children having more global externalizing problems (mixed hyperactive and aggressive symptoms), and all but two (Gorenstein, Mamato, & Sandy, 1989; Johnson, 1991) used clinic-referred samples. Differences in ages, gender composition, and other important subject variables also differed across studies, further limiting the comparison of their results. Moreover, these studies differed in their sample sizes, and hence their relative power to detect group differences on these measures. Despite these important methodological differences, a fairly consistent pattern emerges for some measures while for others the findings are negative or confusing. The tests used are described in greater detail in the report on our own study later in this paper. The Wisconsin Card Sort Test (WCST) has been used in 13 previous studies. Eight of the 13 found significant deficits in A D D / + H children relative to control children on WCST measures traditionally thought to be most sensitive to frontal lobe pathology, these being perseverative responses, perseverative errors, and number of categories correctly achieved. Although Johnson (1991) found A D D / + H adolescents to place in the clinically impaired range in perseverative responses, they actually had fewer such responses than did A D D / - H adolescents. In contrast, Grodzinsky and Diamond (1990) found only that A D D / + H children displayed more trials to complete the first category and tended (p < .06) to have more failures to maintain set than normal children but found no differences on any other measures. Of the five studies finding no deficits in ADD/+H, three used adolescent subjects whereas none of the seven affirmative studies did so. This suggests that age of the subjects may be an important variable in accounting for some of the negative findings. Three studies (Boucagnani & Jones, 1989; Chelune, Ferguson, Koon, & Dickey, 1986; Grodzinsky & Diamond, 1990) found significant reductions in these same WCST measures with age such that older A D D / + H subjects were considerably less deviant from nor-

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mal than their younger counterparts. The failure of Loge, Staton, and Beatty (1990) to find differences on the WCST could be due to their use of nonclinical subjects and smaller sample size. The negative findings by Grodzinsky and Diamond (1990), however, are not so readily explained. They did use young, elementary-age subjects and sufficient sample sizes for adequate statistical power. Even so, most studies suggest that the WCST may be sensitive to deficits in A D D / + H but only in children, rarely in adolescents. Perhaps some of the insensitivity of this measure results from its assessing primarily functions of the dorsolateral frontal cortex (Milner, 1963) whereas A D D / + H seems more of a dysfunction in the orbital prefrontal-striatal-limbic interconnections (Benson, 1991; Heilman et al., 1991; Lou, Henriksen, & Bruhn, 1990). The subtle nature of the dysfunction in frontal lobe functions in A D D / + H may also be such that, with maturation, the extent of impairment becomes considerably less detectable on tests of gross damage to this region. The Stroop test was used in six studies. Five found A D D / + H children to be more impaired on this test, particularly the interference part, relative to normal children. It appears to be the time measure more than the error score which best discriminates ADD/+H and control children. Only Cohen et al. (1972) did not find differences between their A D D / + H and normal children on this test. Perhaps this is because they used hyperactive children. followed over 5 years into adolescence, some of whom were no longer hyperactive, whereas the other studies assessed subjects at their clinical referral and diagnosis. Contradicting this was the Hopkins et al. (1979) findings of significant group differences with this same sample in young adulthood, at which time a considerably larger sample was tested. These findings indicate that the Stroop may be sensitive to the frontal lobe impairments hypothesized to exist in ADD/+H. Verbalfluency, particularly as measured by the Controlled Oral Word Association Test (COWAT), has been described in the clinical neuropsychology literature as an ability easily disrupted by frontal lobe injuries (Crockett, Bilsker, Hurwitz, & Kozak, 1986). Five previous studies of A D D / + H children used this measure and found quite mixed results. Three (Fischer, Barkley, Edelbrock, & Smallish, 1990; Loge et al., 1990; McGee et al., 1989). found no significant impairments relative to normal children on any measures from this test while Felton, Wood, Brown, and Campbell (1987) found impairments in both their reading-disabled (RD) and A D D / + H children. Grodzinsky and Diamond (1990) found reduced scores only on the letter portion of the test in the A D D / + H group compared to normals. The finding that RD children may have problems with this test calls into doubt its specificity for A D D / + H or for abnormalities of frontal lobe functions, which are not thought to be impaired in RD. That a study using a

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nonverbal form of this test (Loge et al., 1990) also proved negative for A D D / + H raises further doubts about its assessing the cognitive problems specific to ADD/+H. The discrepant findings across studies using this test await a sensible explanation. Meanwhile, they clearly warrant caution in using the test as a specific measure of frontal lobe dysfunction in A D D / + H children. The findings for five studies that used the Rey-Osterrieth test also call into considerable doubt any specificity it may have for ADD/+H. Three studies (Barr, Douglas, & Sananas, 1990; Douglas & Benezra, 1990; Grodzinsky & Diamond, 1990) found their ADD/+H children to perform this figure drawing task more poorly than normal children. Douglas and Benezra, however, did not find differences between their RD and A D D / + H subjects on this test, a more critical test of specificity of the findings to ADD/+H. McGee et al. (1989) found differences from their control group only on the memory measure and only in A D D / + H children who had comorbid RD. Similarly, Moffitt and Silva (1988) found only their A D D / + H subjects who were seriously delinquent to have deficits on this task whereas those A D D / + H subjects who were not delinquent were not different from the non-ADD/+H subjects. The ADD/+H delinquents had significant impairments in many other areas of cognitive function relative to the purely A D D / + H and purely delinquent subjects. This suggests that cognitive impairments other than those seen in ADD/+H, such as those seen in RD, other learning disabilities (LD), or even conduct disorder (CD), may affect performance on this test. Nine studies used variations of the Trail Making Test (TMT) with A D D / + H children. Of these, five did not find A D D / + H children to have impairments on the time to complete this task. The affirmative studies also had quite mixed results. Gorenstein et al. (1989) found their ADD/+H children to perform only Part B of this test more slowly than normal. Chelune et al. (1986) found only the error score, rather than the time score, on the Color Forms version of this test to discriminate the A D D / + H children from the normal controls. Shue and Douglas (1989) found more errors on Part A and both greater time and error scores on Part B in their A D D / + H compared to normal children. Boucagnani and Jones (1989) found A D D / + H children to be deficient only on the time measure of Part B. Quite the opposite pattern was noted in Johnson's (1991) study of ADD adolescents: ADD/-H teens actually performed more slowly on Part B than did A D D / + H teens. Age might be important in accounting for some of the discrepant results, as Grodzinsky and Diamond (1990) found significant reductions with age on the standard version of this test such that smaller differences from normal were noted in older than younger A D D / + H children. How-

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ever, while three of the negative studies were with adolescents consistent with such an hypothesis, two other disconfirming studies used young children implying that age effects alone cannot explain the discrepant results. More likely, the version of the test used seems just as important. Four of the studies used the standard version of the test with 6--11 year olds and three of these found the time score to differentiate their groups. In contrast, neither study using the Color Forms version found such group differences. Thus, both age and test version may interact to partly explain the different results across studies. Patterns of predominantly negative findings have been noted for the Grooved Pegboard Test (four studies, all negative) and for maze-like tests, such as the Porteus or Wechsler Intelligence Scale for Children-Revised (WISC-R) Mazes (five studies, three negative). The weight of the evidence to date is against these two tests being reliably sensitive to the neurocognitive deficits seen in A D D / + H children. Variations of the Hand Movements test have been used extensively in adult clinical neuropsychology as a measure of frontal lobe impairment (Lezak, 1983; Luria, 1966). Both Breen (1989) and Mariani (1990) found their A D D / + H children to be more impaired on this task than their normal control children. Although these results require replication, especially using non-ADD clinical control groups, they imply potential promise for the sensitivity of this measure to the deficits related to A D D / + H . Two studies to date have used the Go-No-Go test with A D D / + H children. The test merely requires the subject to display a simple motor response to one cue, the go stimulus, while inhibiting the response to a n o t h e r cue, the no-go stimulus. T r o m m e r , H o e p p n e r , Lorber, and Armstrong (1988) cited evidence that the test is quite sensitive to frontal lobe lesions in adults, possibly to more right than left hemisphere injuries (Heilman et al., 1991). Trommer et al. (1988) found that A D D children ( + H and - H groups collapsed together) made more total errors and more multiple errors than normal children. Shue and Douglas (1989) also noted more such errors in their A D D / + H than normal children. A recent study has also shown this test to be sensitive to dose effects of methylphenidate in A D D / + H (Trommer, Hoeppner, & Zecker, 1991). These findings suggest some promise for this measure in detecting the behavioral disinhibition associated with A D D / + H . Such inhibition is probably mediated by the prefrontal cortex (Trommer et al., 1988). To summarize, the CPT, Stroop (interference), Hand Movements, and Go--No-Go tests appear to have some reliability in detecting differences between A D D / + H and normal groups of children. The WCST may have some sensitivity in detecting differences between A D D / + H and normal controls but only for 6- to ll-year-old children. Similarly, the TMT time

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score shows some promise for this same age range but only for the standard version (Part B) rather than the Color Forms version. Despite such promising findings, most of these studies failed to use non-ADD clinical control groups to provide a more critical test o f the sensitivity of these measures for specifically ADD/+H. To date, only the CPT seems to reliably make such distinctions. Most of these tests have in common the assessment of the ability to inhibit motor responses on demand, especially while being required to perform a competing response. Such response inhibition is believed by many to be mediated by the frontal lobes and particularly the orbital-prefrontal and medial-prefrontal areas and their rich connections to the striatum (Benson, 1991; Heilman et al., 1991; Stuss & Benson, 1986). By inference, A D D / + H seems best characterized as a disinhibition disorder arising out of a dysfunction of these brain regions (Barkley, 1990; Quay, 1988). Studies Comparing ADD/ +H with ADD/-H Despite the apparent commonalities in symptoms among A D D children, those so diagnosed are actually not homogeneous, having a diversity of related psychiatric symptoms, family backgrounds, developmental courses and responses to treatments (Barkley, 1990). Given this heterogeneity, efforts have been made to identify methods of subtyping this disorder into more homogeneous, clinically meaningful subgroups. One of these methods is founded on the extent of overactivity, as proposed in the DSM-III (APA, 1980), separating A D D children into those with and without hyperactivity. Several early descriptive studies of these subtypes found few significant differences between A D D / + H as compared to ADD/-H children (Maurer & Stewart, 1980; Rubinstein & Brown, 1984). Others reported that A D D / + H children were more aggressive, more rejected by peers, had lower self-esteem, and were more impaired in cognitive and motor test performance than ADD/-H children (Berry, Shaywitz, & Shaywitz, 1985; King & Young, 1982). In contrast, the ADD/-H children were described by teachers as anxious, daydreamy, lethargic, and sluggish relative to A D D / + H children (Edelbrock, Costello, & Kessler, 1984; Lahey, Schaughency, Hynd, Carlson, & Nieves, 1987; Lahey, Schaughency, Strauss, & Frame, 1984). Several studies have compared these subtypes on academic tests with mixed results. Most studies found no substantial differences between them on achievement or in their percentage who were LD. Both subtypes were more impaired than a normal control group (Barkley, DuPaul, & McMurray, 1990, 1991; Carlson, Lahey, & Neeper, 1986; Lahey, 1988). In con-

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trast, a few small studies have found preliminary indications of greater LD in the group with ADD/-H (Edelbrock et al., 1984; Hynd et al., in press-b). Others (Carlson, et al., 1986; Neeper, 1985) have examined the performance of these subtypes on a small set of neuropsychological tests, such as tests of visual-motor integration, the Stroop test, a rapid naming task, and tests of language functioning. No differences were found between the subtypes of ADD on these tasks but both subtypes differed in some respects from a normal control group. Schaughency et al. (1989) compared A D D / + H with ADD/-H children and a clinical control group of children without ADD on the Luria-Nebraska Neuropsychological B a t t e r y Children's Revision ( L N N B - C R ) and also found no differences between the subtype groups; nor did either subtype group differ from the control group. Lastly, Trommer et al. (1988) found that both A D D / + H and ADD/H children had more total errors and more multiple errors on the Go-NoGo test than did normal control children. Surprisingly, the A D D / - H children showed more commission errors on the first trial than did A D D / + H children. While these studies seem to suggest that these subtypes have similar cognitive deficits and, therefore, share a common neuropsychological disturbance, sufficient flaws exist in the methodologies of the studies to make them less than definitive on this issue. Further studies of potential neuropsychological differences between these subtypes, however, are worthwhile for several reasons. First, prior studies, noted above, have shown that the behavioral, emotional, and social characteristics of these two ADD subtypes are quite different (Barkley et al., 1990; Carlson, 1986; Lahey, Schaughency, Frame, & Strauss, 1985). The pattern of psychiatric disturbances in their biological relatives is also different, with A D D / + H children having more conduct problems, alcohol abuse, and hyperactivity among their relatives and ADD/-H children more anxiety disorders and LDs among their biological relatives (Barkley et al., 1990). This implies that these subtypes may be distinct childhood disorders despite both having deficits in attention. Second, several studies of the attention problems of these ADD subtypes indicate that their deficits may be in different components of attention. A D D / + H children may have more problems with sustained effort or "resource allocation" during tedious, boring tasks while ADD/-H children may have a more "sluggish cognitive tempo" (perceptual-motor processing speed) or an impairment in focused attention (Barkley et al., 1990; Lahey et al., 1988; Hynd et al., in press-b; Sergeant & Scholten, 1985a, 1985b). Given that current neuropsychological models of attention suggest distinct anatomical localizations for these different components of attention (sustained vs. focused; Mesulam, 1990; Mirsky, 1987; Posner,

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1988), one would expect them to have different neuropsychological sequelae. Finally, as reviewed earlier, several recent studies have indicated that A D D / + H children seem to have deficits on some neuropsychological tests of various frontal lobe functions, particularly response inhibition, relative to normal children (Chelune et al., 1986; Gorenstein et al., 1989; Grodzinsky & Diamond, 1990; Heilman et al., 1991; Mariani, 1990). Furthermore, several studies using measures of cerebral blood flow (Lou et al., 1990) and CT (computerized axial tomography) scan (Hynd, SemrudClikeman, Lorys, Novey, & Eliopulos, 1990) have noted diminished blood flow and brain matter, respectively, in the prefrontal areas of these children. Yet only three studies to date have examined possible differences between these ADD subtypes on neuropsychological tests pertaining to frontal lobe functions. One (Carlson et al., 1986) employed the Stroop test, as noted above, and failed to find differences between these ADD subtypes. This is hardly a thorough or even representative examination of the diversity of functions thought to be subserved by the frontal lobes (Stuss & Benson, 1986). The second study used the L N N B - C R (Schaughency et al., 1989), which contains no scales that specifically assess frontal lobe functions and, in fact, intentionally excluded them in its development. The third study (Trommer et al., 1988), noted above, found both types of ADD children to have more response disinhibition (commission errors) than normal children on the Go-No-Go test. The ADD/-H subjects displayed more such errors than the ADD/+H children on the first trial of this multitrial task. In view of these mixed results, a more comprehensive study seems indicated. A major problem with past comparisons of these ADD subtypes is their reliance on clinicians' judgments using the DSM-III criteria for these two subtypes. Factor analyses of the DSM-III item lists for attention, hyperactivity, and impulsivity have not found these items to cluster into the same behavioral dimensions as they are listed in the DSM-III (Lahey et al., 1988). Items of impulsivity, in fact, correlate highly with those of hyperactivity, often forming a single dimension. Artificially separating subjects into inattentive-impulsive (ADD/-H) and inattentive-impulsive-hyperactive (ADD/+H) groups based on DSM-III item lists may result in relatively impure subgroups of ADD that are not distinctly different on the most important symptom of ADD/+H, that being impulsivity or disinhibition. The findings noted above for the Go-No-Go test in which both subtypes had greater errors could be accounted for by such an explanation given that Trommer et al. (1988) used the DSM-III item lists. Other studies have used nonclinical samples of children defined as ADD only as a result of relatively high scores on teacher rating scales that typically

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would not be considered clinically deviant. The extent to which their results are representative of clinic-referred children with seriously deviant ADD symptoms is questionable. Equally as important, past studies of neurocognitive deficits in these subtypes did not employ a control group of LD children. This is a critical control group in view of the large minority of ADD children (20 to 50%) who have co-existing primary LDs (Barkley et al., 1990; Lambert & Sandoval, 1980). It is conceivable that differences between these ADD subtypes or between ADD and normal children on such tests could be due to the presence and degree of co-morbid LDs rather than to the ADD itself. Similarly, different rates of co-morbid CD associated with each ADD subtype could also confound the interpretation of differences between these groups on neuropsychological measures. A D D / + H children have been repeatedly found to have considerably higher rates of CD than ADD/-H children. Although CD has not been reliably associated with cognitive deficits apart from those due to A D D / + H (Barkley, McMurray, Edelbrock, & Robbins, 1989), the aforementioned study by Moffitt and Silva (1988) did find more numerous neuropsychological impairments in ADD adolescents who were delinquent than in those who were not. This suggests that the degree of CD in the ADD subtypes must be controlled for in neuropsychological studies if the differences found between them are to be more confidently attributed to the hypothesized distinctions in the nature of their attention problems. It was the goal of the study that follows to conduct a preliminary evaluation of possible differences between these A D D subtypes using a more thorough battery of measures of frontal lobe functions than in past such subtype comparisons. The study used clinic-referred A D D children, an empirical criterion for creating the ADD subtypes rather than the unsatisfactory DSM-III criteria, and a control group of non-ADD LD children besides a normal control group, and statistically controlled for the differences among these groups in their degree of CD.

METHOD Subjects We used four groups of subjects: 12 boys with A D D / + H , 12 boys with ADD/-H, 11 boys with LD, and 12 boys in the community control group who were a subset of those participating in our larger investigation into social, emotional, behavioral, academic, and medical differences between these A D D subtypes (Barkley et al., 1990). The selection criteria used to group these subjects were identical to those described in detail in that larger study.

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Procedures Mothers of the children completed a packet of child behavior rating scales, as did the children's teachers, to determine eligibility for participation in the study. This packet included the Child Behavior ChecklistTeacher Report Form (CBCL-TRF). Eligible children and their mothers were then seen on a single day during which all dependent measures were collected in the same standardized order by a research assistant who was not blind to the group membership of these children. At the end of the evaluation, parents were paid $25 as a stipend, and children were given a $2 gift certificate to a local ice cream restaurant. Children were not told of these gift certificates until the end of the evaluation.

Screening Measures Child Attention Profile (CAP; Barkley, 1990). This rating scale was used to select and sort the subjects into those with and without ADD. The CAP scale is a 12-item questionnaire derived from the items on the CBCL-TRF ( A c h e n b a c h & Edelbrock, 1986) Inattention and N e r v o u s - O v e r a c t i v e scales. Seven attention items and five overactivity items were extracted to produce a two-factor rating scale. These items were selected for having the highest loadings on their respective scale while correlating to a low degree with the other scale. It, therefore, seemed that the CAP would prove useful in an empirically based approach to subtyping of A D D children into those with and without hyperactivity. Normative data for the CAP were derived from the same sample used to construct the norms for the CBCL-TF. The scale has excellent psychometric properties (Barkley, 1990; Barkley et al., 1990) and has been shown to be highly sensitive to dose effects of stimulant drugs with A D D children (Barkley et al., 1989). 2. Wechsler Intelligence Scale for Children-Revised (WISC-R). T h e standard score for the full-scale IQ was used in the analyses of group differences. To estimate IQ, the split-half form of the WlSC-R (Sattler, 1982) was used. Dependent Measures of Frontal Lobe Functions 1. Continuous Performance Test (Gordon, 1983). This is a 9-min vigilance test during which numbers are presented on a display screen at the rate of one per second. In our study the stimulus stayed on for 800 msec with a 200 msec delay between stimulus presentation. T h e r e were

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45 target pairs (1 then 9) presented during testing. Scores were the number of omissions and number of commissions. 2. Grooved Pegboard Test (Reitan & Wolfson, 1985). This is a commonly used measure of fine motor speed and agility in clinical neuropsychology. T h e child is asked to place pegs with his d o m i n a n t , t h e n his nondominant hand, into a 5-in. x 5-in. pegboard containing 25 slotted holes angled in different directions. The times taken by the subject to complete the task with each hand serve as the dependent measures.

3. Controlled Word Association Test (COWAT; Benton & Hamsher, 1978). This test involves the examiner asking the subject to make verbal associations to different letters of the alphabet beginning with F (or A or S) (from which it is often referred to as the verbal fluency or FAS test) excluding proper nouns, numbers, and the same word with a different suffix. In our study, a modification was added in which the subject was then asked to first name all of the words he could think of within the category of animals, followed by a trial for the category of foods. One minute was allowed for each stimulus letter or semantic category. Three scores were derived: (a) the sum of all the acceptable words produced within the total time limit for all three letters, (b) total acceptable words for the animal category, and (c) total acceptable words for the food category. 4. Hand Movements Scale (Kaufman & Kaufrnan, 1983). This is an adaptation of a clinical task developed by Luria (1966) for evaluating the ability to imitate progressively longer sequences of skilled hand movements. The child's score is the number of sequences of such hand movements successfully imitated which then is converted to a standard score. 5. Porteus Mazes (Porteus, 1965). This is a pencil-and-paper maze-tracing task requiring planning and organizational skills as well as fine motor dexterity. Two scores are obtained from this test: (a) q u a n t i t a t i v e - a mental age score based on the number of repeated trials with a maximum score of seventeen; and (b) q u o t i e n t - a test quotient based on the mental age score (Buros, 1972). 6. Rey--Osterrieth Complex Figure (see Lezak, 1983). This is a papera n d - p e n c i l task r e q u i r i n g planning and v i s u a l - s p a t i a l - c o n s t r u c t i o n a l abilities and is sensitive to deficits from frontal lobe injuries (Lezak, 1983). The task requires the subject to copy a geometric shape. The Waber and Holmes (1985) scoring procedure was used, yielding scores for organization (five levels) and style (four categories). Only the organization score served as a dependent measure. 7. Stroop Color-Word Test (Stroop, 1935). The test contains three parts, each having a separate card containing 5 columns of 20 items. First the subject is asked to read a list of color names (blue, red, and green) in black ink as rapidly as possible. Then the subject is required to name

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Table II. Demographic and Initial Selection Information for Each Subject Group a ADD+H (1)

Measure Age (years) Grade (years) WlSC-R Vocabulary WlSC-R Block Design IQ (WISC-R) Hollingshead Index CAP Inattention

ADD/-H (2)

LD (3)

Normal (4)

F/X2 p < .05

Contrasts

Mean SD

9.2 1.3

9.1 1.4

9.9 1.5

9.1 1.4

0.80

-

-

Mean SD

3.3 1.6

2.9 1.4

3.4 1.6

3.1 1.2

0.21

-

-

Mean SD

10.8 3.1

10.4 3.0

9.2 3.1

12.3 3.4

1.92

-

-

Mean SD

11.8 3.2

11.8 3.1

10.5 2.4

11.1 1.9

0.61

Mean SD

107.7 11.2

106.3 14.8

99.0 11.9

109.8 12.8

1.53

Mean SD

51.7 27.2

49.1 23.4

54.5 24.2

43.3 26.7

0.41

Mean SD

11.9 1.8

9.6 2.0

3.5 3.6

0.9 1.4

50.75

.001

1 > 2 > 3 > 4

8.8 1.4

2.6 1.4

1.7 2.1

1.6 2.2

43.62

.001

1 > 2, 3 , 4

11.8 2.3

5.4 1.8

1.5 2.0

0.3 0.9

97.75

.001

1 > 2 > 3, 4

67.8 10.5

56.8 8.8

55.1 4.2

55.4 1.7

13.37

.001

1 > 2, 3 , 4

91.6

16.7

0.0

0.0

20.31

.001

1 > 2, 3 , 4

CAPOveractivity Mean SD No. A D H D symptoms Mean SD CBCL-TRF Aggression Mean SD % Diagnosed ADHD

a A D D / + H = attention deficit disorder with hyperactivity; A D D / - H = attention deficit disorder without hyperactivity; LD = learning-disabled; Normal = normal control subjects; SD = standard deviation; F/~2 = the F test or chi-square value, as appropriate; p < = probability value for those univariate analyses of variance which reached a level of statistical significance (p < .05); Contrasts = the results of palrwise contrasts using Newman-Keuls tests in which a contrast reached statistical significance (p < .05); the numbers represent those assigned to each group as shown in parentheses below each group name; WISC-R = Wechsler Intelligence Scale for Children-Revised; CAP = Child Attention Profile; A D H D = attention deficit hyperactivity disorder as defined in DSM-III-R; CBCL-TRF = Child Behavior Checklist-Teacher Report Form.

c o l o r e d p a t c h e s o f i n k a s r a p i d l y a s p o s s i b l e . F i n a l l y t h e s u b j e c t is r e q u i r e d t o n a m e t h e c o l o r o f i n k i n w h i c h a w o r d is p r i n t e d a s r a p i d l y a s p o s s i b l e . T h i s is t h e " i n t e r f e r e n c e "

test, as the words are color names

of a different color. Each of the three

p r i n t e d in i n k

p a r t s is t i m e d f o r 45 s e c . T h e s c o r e

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179

is the time needed to complete each portion and the number of corrected responses. 8. Trail Making Test (A & B) (Reitan & Wolfson, 1985). The Intermediate version was used and comprises two parts: A and B. In Part A, the subject connects a series of numbered circles distributed arbitrarily about a page. Part B comprises circles that contain letters or numbers scattered randomly across the page. The subject is to alternate connecting numbers and letters in ascending order until the end of the sequences. The scores are the time taken to complete each part and the number of errors made by the subject. 9. Wisconsin Card Sorting Test (WCST). The test consists of 128 cards containing sets of geometric designs that vary according to color, form, and number. The subject is given four cards and then asked to sort the remaining deck of cards using feedback provided by the examiner. Scoring includes the total categories achieved, perseverative errors, percent of responses that are correct, failures to maintain the set of responses, perseverative responses, nonperseverative responses, and number of responses to complete the first category (Heaton, 1981).

RESULTS Results for the demographic information and the selection criteria are shown in Table II. The groups were compared on these measures using univariate analyses of variance (ANOVA). Significant differences among the groups were found on the teacher ratings of inattention and overactivity from the CAP (p < .001). This was expected given that this scale was used to define the groups. The groups also differed in their degrees of aggression or conduct problems as rated by teachers on the CBCL-TRF. The groups did not differ significantly in the children's age or grade in school, performance on the IQ subtests or full-scale IQ, or parents' socioeconomic status as assessed by the Hollingshead Two-Factor Index of Social Position. T h e significant finding for the CAP I n a t t e n t i o n scale was subsequently analyzed using Newman-Keuls pairwise comparisons which ind i c a t e d t h a t the A D D / + H g r o u p was r a t e d as significantly m o r e inattentive than the other three subject groups. The A D D / - H group was also rated as significantly more inattentive than the LD and normal groups. These findings were expected given the use of the CAP to select these two groups. The L D group, however, was also rated as significantly more inattentive than the normal control group despite the criterion that both of these two control groups be below the 84th percentile on this

Barkley, Grodzinsky, and DuPaul

180

Table III. Neuropsychological Tests of Frontal Lobe Functions by Group a ADD/+H ADD/-H (1) (2)

Measure CPT, commission errors M

2.25

-

-

9.3 8.4

12.1 9.4

4.3 3.9

2.6 1.8

5.51

.01

1 > 4, 2 > 3, 4

57.4 18.4

52.1 25.9

65.5 26.5

56.6 22.5

0.62

-

-

58.2 24.4

55.3 21.8

71.2 30.0

65.3 30.3

0.76

-

-

20.3 7.4

27.1 11.6

22.2 7.5

17.7 5.4

2.15

-

-

60.1 31.5

77.3 40.6

51.4 25.1

45.4 27.6

1.68

-

-

92.9 14.1

93.3 12.2

94.5 5.0

103.9 13.2

1.39

-

-

SD M

11.5

12.9 3.0

12.3 3.3

-

-

2.7

10.7 2.5

1.11

SD

118.8 17.2

117.3 14.2

123.8 16.1

120.7 15.2

0.46

-

-

8.7 2.2

6.8 1.9

7.3 1.5

9.2 3.1

1.82

-

-

47.1 5.6

45.8 7.9

45.3 8.1

52.8 4.7

3.39

.03

43.9 5.8

44.7 5.4

43.7 7.5

48.1 3.8

1.06

-

44.3 5.3

45.8 7.2

44.8 6.3

51.7 4.7

4.33

.01

19.4 9.1

16.8 2.2

20.4 2.1

23.2 5.6

2.84

.05

-

12.8 2.5

12.4 3.3

13.0 2.8

14.8 4.4

0.49

-

-

10.0 2.0

10.5 3.1

12.0 4.6

14.4 4.9

1.79

-

-

M

M

SD M

SD M

SD Hand Movements Porteus Mazes, age Porteus Mazes, quotient

M

M

SD Rey-Osterrieth, age

M

SD Stroop, words

M

SD Stroop, colors

M

SD Stroop, interference

M

SD COWAT, FAS letters

M

SD COWAT , animals

M

SD COWAT, foods

Contrasts

8.3 8.0

SD

Trails Part B, time

p < .05

5.0 3.5

Pegboard, d omin ant (sec) M

Trails Part A, time

F

27.9 43.0

SD

Pegboard, n ondomin ant

Normal (4)

35.6 45.9

SD CPT, omission errors

LD (3)

M

SD

4 > 1, 2, 3

-

4 > 1, 2, 3

Attention Deficit Disorder

181 Table III. Continued

ADD/+HADD/-H (1) (2)

Measure COWAT, names WCST, No. correct WCST, total errors WCST, categories WCST, Persev. errors WCST, percent WCST, Nonpers. errors WCST, Persev. responses WCST, failures of set WCST, No. to 1st category

LD (3)

Normal (4)

F

p < .05

Contrasts

M SD

13.0 5.1

11.3 5.4

13.4 4.0

14.4 6.3

0.63

-

-

M SD

70.5 13.3

64.3 16.2

69.6 15.1

72.1 19.0

0.34

-

-

M SD

51.4 20.2

54.2 26.9

51.2 22.1

47.8 25.3

0.40

-

-

M SD

3.9 1.6

3.7 2.1

3.9 1.6

4.4 2.2

0.49

-

-

M SD

29.4 15.5

38.2 26.5

32.6 21.8

24.9 16.4

0.71

-

-

M SD

23.4 11.6

30.6 19.8

26.1 16.4

19.9 12.3

0.77

-

-

M SD

22.0 10.9

16.0 10.4

18.5 9.8

22.8 11.2

1.26

-

-

M SD

34.2 20.1

46.3 34.6

36.8 30.2

27.1 19.4

0.94

-

-

M SD

1.0 1.1

0.6 0.9

1.2 1.5

0.9 0.7

1.07

-

-

M SD

20.8 21.9

12.1 5.9

25.4 34.8

10.5 3.6

1.56

-

-

a A D D / + H = attention deficit disorder with hyperactivity; A D D / - H = attention deficit disorder without hyperactivity; LD = learning-disabled; Normal = normal control subjects; M = mean for raw scores; SD = standard deviation; p < = probability value for those univariate analyses of covariance tests which reached a level of statistical significance of p < .05; Contrasts = the results of pairwise contrasts using Newman-Keuls tests in which a contrast reached statistical significance (p < .05); CPT = Continuous Performance Test; C O W A T = Controlled Oral Word Association Test; FAS stands for alphabetical letters F, A, and S; WCST = Wisconsin Card Sort Test; Persev. = perseverative; Nonpers. = nonperseverative.

scale.

Nevertheless,

nificant

levels

symptoms group

nor

from for

of these

of ADD,

(DSM-III-R), ANOVA

none

none any

the normal

the

was rated

did CAP

of

LD

received them

control

Overactivity

as significantly

children

more

a clinical

differ

children scale

met

in the

our

criteria

diagnosis

of ADHD

number

of ADHD

(see below). indicated

active than

for sig-

that

the other

The the

significant ADD/+H

three

groups,

182

Barkley, Grodzinsky, and D u P a u l

which did not differ among themselves. This was also expected given the use of the CAP for choosing the A D D / + H group. The number of A D H D symptoms from the DSM-III-R endorsed for each group along with the percentage of each group meeting all diagnostic criteria for A D H D are also shown in Table II. As expected from the s e l e c t i o n c r i t e r i a , the A D D / + H g r o u p had significantly m o r e symptoms of A D H D by parent report than the other three groups (p < .001). The A D D / - H group was also rated as having significantly more of these symptoms than the L D and normal control groups, which were not significantly different from each other. The vast majority of A D D / + H subjects (91.6%) met criteria for a diagnosis of A D H D while only 2 (16.7%) of the A D D / - H children and none of the L D or normal children did so. The significant difference among the groups on the C B C L - T R F Aggression scale was subsequently analyzed by Newman-Keuls comparisons which found that A D D / + H children were rated significantly higher on this scale than the other three groups. T h e neuropsychological measures were analyzed using one-way analyses of covariance (ANCOVA) with the T score from the C B C L - T R F Aggression scale serving as the covariate. As noted earlier, this seems advisable given the possibility that neuropsychological differences found among the groups might be due to the above noted differences in the degree of co-morbid CD in these groups. Since teacher ratings of inattention and overactivity were used to form the subject groups, it seemed most appropriate to use teacher ratings of aggression, rather than parent ratings, as the covariate. The raw means and standard deviations for the dependent measures are shown in Table III. Significant overall group differences (p < .05) were noted on the following measures: Omission errors from the CPT, the word and interference scores from the Stroop test, and the FAS portion of the verbal fluency test. The measures on which there were significant A N C O V A s were further evaluated using Newman-Keuls pairwise contrasts. The contrasts for the Omission score from the CPT indicated that both A D D groups had significantly more errors of omission than the normal control group. The two A D D subtypes did not differ between themselves on this test. On the Stroop test, the contrast analyses showed that both A D D groups and the LD group scored significantly lower than the normal control group on the word reading portion (part I) and on the interference portion (part III) of this test. Despite the overall A N C O V A being significant, the pairwise contrasts for the FAS portion of the verbal fluency test revealed no contrasts to be significant at the p < .05 level.

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183

DISCUSSION

Our findings are admittedly limited by the small sample sizes and the resulting reduction in statistical power. With this in mind, the results of this preliminary exploration of frontal lobe functioning in A D D / + H and ADD/-H children indicated few differences between these ADD subtypes. Both ADD groups made significantly more errors of omission on the CPT than the normal control children. Both ADD groups also had lower scores on the word and interference portions of the Stroop test than the normal children, but so did the non-ADD LD group. Nevertheless, the ADD subtypes failed to show any significant differences from each other or the normal or LD control groups on the Pegboard, Hand Movements, Porteus Mazes, Rey-Osterrieth, Trails, or WCST. A unique pattern of frontal lobe deficits for each ADD subtype was, therefore, not established in this preliminary study but a replication of this study using larger samples of children would be in order before accepting this conclusion unequivocally. Even if confirmed, findings on other psychological tests of nonfrontal lobe abilities from other studies continue to suggest the possibility of a problem with perceptual-motor processing and speed in children with ADD/-H not seen in A D D / + H (Barkley et al., 1990; Hynd et al., in press-b; Johnson, 1991; Lahey et al., 1988; Sergeant & Scholten, 1985a, 1985b). Although the pattern of findings reviewed earlier suggests that the Stroop test may be detecting the problems of behavioral disinhibition that are attributed to A D D / + H children (Heilman et al., 1991), the findings of this study raise some doubt about this interpretation. The ADD/-H and LD children performed significantly more poorly on both the word reading and interference portions of this test yet neither of these groups has been previously characterized as impulsive or uninhibited nor were they rated so by parents or teachers in this study. This suggests that poor performances on the Stroop test may be due to several factors related to LDs, such as scanning, rapid naming, and general reading dysfluency (Lezak, 1983). The failure to find significant group differences between A D D / + H and normal children on the Hand Movements test contradicts two studies reviewed earlier using this test. Similarly, the WCST was not useful in discriminating the groups, unlike most other studies using similar age children. Again, the limited sample size could have accounted for our nonsignificant results. At best, the pattern of findings across the literature on frontal lobe deficits in ADD//+H indicates a problem of inhibitory control in this disorder as documented by the CPT and WCST. The pattern for other presumably frontal lobe tests is quite inconsistent and highly dependent on the measures

184

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used and age range of the subjects. Other methodological differences across studies are also likely to have contributed to this predicament. One may have been the extent to which co-morbid LD and CD account for some earlier findings misattributed to ADD. An important contrast in this study was between the ADD groups and the non-ADD LD control group. This contrast is critical given that a significant minority of ADD children are likely to have LD (August & Garfinkel, 1990; Barkley et al., 1990) and that such LDs may result in impaired performances on many of the neuropsychological tests used here (McGee et al., 1989). The ADD groups differed from the LD group only on omission errors from the CPT. This suggests that the impairments found in the ADD groups on other measures (e.g., Rey-Osterrieth, Stroop, and Trails) may well be a function of other sources of variance instead of or in addition to ADD, perhaps stemming from the extent of LD or CD in the ADD groups. Failure to control for such co-morbid conditions may lead to the erroneous conclusion that the deficits found in the ADD children are attributable to their ADD when, in fact, they are due to the overlap with the other co-morbid disorders (McGee et al., 1989). Unfortunately, most studies have failed to employ such controls and have likely made this mistaken attribution. Also of import is the fact that all of the tests reviewed here were drawn from the literature on adult neuropsychology and, consequently, may not be so easily extended downward to child populations as equally valid measures of frontal lobe functions (Taylor, Fletcher, & Satz, 1984). Even if these tests are ultimately validated as assessing frontal lobe lesions in children, they still may prove insensitive to the types of problems seen in A D D / + H . This may be due, in part, to the fact that lesions have considerably different effects on cognitive development when they occur at different developmental periods. Validating these measures on children with demonstrable frontal lobe damage occurring in childhood does not mean the tests can assess the more subtle deficits in ADD that may date from pre- or perinatal events or from genetic contributions (Barkley, 1990). The totality of findings suggest that future neuropsychological research on ADD and its subtypes would have more promise if it (a) adopted a more consistent and empirical method of establishing the diagnosis of A D D and classifying the subtypes in place of DSM-III item lists; (b) used clinically deviant subjects; (c) controlled for the effects of LD, CD, and other co-morbid disorders on the neuropsychological measures; (d) focused on the more severely impaired childhood than adolescent ADD population; (e) concentrated on a finer analysis of the types of errors made on tests of inhibition (Halperin et al., 1990); and (f) included measures of focused attention and perceptual-motor speed rather than just measures of the more global frontal lobe functions evaluated here.

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