Journal of Attention Disorders

http://jad.sagepub.com Distinct Response Time Distributions in Attention Deficit Hyperactivity Disorder Subtypes
Laurent Querne and Patrick Berquin J Atten Disord 2009; 13; 66 originally published online Aug 25, 2008; DOI: 10.1177/1087054708323006 The online version of this article can be found at: http://jad.sagepub.com/cgi/content/abstract/13/1/66

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Distinct Response Time Distributions in Attention Deficit Hyperactivity Disorder Subtypes

Laurent Querne
Amiens University Medical Center, France

Journal of Attention Disorders Volume 13 Number 1 July 2009 66-77 2009 SAGE Publications 10.1177/1087054708323006 http://jad.sagepub.com hosted at http://online.sagepub.com

Patrick Berquin
Jules Verne University of Picardy, France
Objective: To address the issue of response time (RT) profiles in hyperactive-impulsive (ADHD-HI), inattentive (ADHD-IA), and combined (ADHD-C) subtypes of ADHD. We hypothesized that children with ADHD-HI should respond more rapidly than children without ADHD and children with ADHD-IA and ADHD-C should respond more slowly than children without ADHD. Method: Four groups (3 ADHD groups and 1 non-ADHD group) each composed of 16 children (7-13 years old) performed a visuospatial choice task. Results: ANOVA indicated very variable RTs for each ADHD subtype when controlling for individual RT. ANOVA performed on RT distribution showed significant differences between the ADHD and non-ADHD groups: biased to fast responses in ADHD-HI and biased to slow responses in ADHD-IA and ADHD-C. Conclusion: The results suggest that response time profiles were abnormal in all ADHD subtypes and were markedly different between children meeting criteria for ADHD-HI and those meeting criteria for ADHD-IA or ADHD-C. (J. of Att. Dis. 2009; 13(1) 66-77) Keywords: ADHD; subtype; variability; distributional analysis

ttention deficit hyperactivity disorder (ADHD) is one of the most common childhood disorders. The symptoms of ADHD, as defined by the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSMIV; American Psychiatric Association, 1994), include inattention, hyperactivity/impulsivity and lead to difficulties in educational, social, and family contexts (Barkley, 1997; Nigg, 2001; Seidman, 2006; Spira & Fischel, 2005). The DSM-IV describes ADHD as a heterogeneous disorder, providing diagnostic criteria for three subtypes: primarily hyperactive/impulsive (ADHD-HI), primarily inattentive (ADHD-IA), and combined type (ADHD-C). Children with ADHD usually have learning difficulties and a low processing speed index as assessed on the Wechsler Intelligence Scale for Children (WISC-IV; Mayes & Calhoun, 2006; Shanahan et al., 2006). The question of ADHD subtypes remained controversial at the present time. The hyperactive/impulsive form is relatively rare, and some authors argue that little empirical evidence is available supporting the validity of this group (Derefinko et al., in press). This form is more often conceptualized as a precursor to the combined subtype because attentional problems appear
66

to emerge during childhood in many children initially meeting criteria for ADHD-HI (Lahey, Pelham, Loney, Lee, & Willcutt, 2005). The controversy surrounding the inattentive form concerns whether this group should be considered to be a distinct disorder (Milich, Ballentine, & Lynam, 2001) rather than an ADHD subtype in which hyperactivity/impulsivity symptoms are absent, or a milder form of ADHD-C (Riccio, Homack, Jarratt, & Wolfe, 2006). A major part of the controversy concerns whether and how the response time profiles differ between subtypes, but few studies have addressed the issue of response time and variability in each of the three ADHD subtypes.

Speed and Variability in ADHD

As pointed out in recent reviews, the overall RT recorded during experimental tasks are typically both slower and more variable in children with ADHD than in
Authors Note: Please address correspondence and request reprints to Professor P. Berquin, Dpartement de pdiatrie, CHU dAmiens, Place Victor Pauchet, F-80054 Amiens Cdex, France.

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Patrick, Laurent / Response Time Distribution in ADHD Subtypes 67

children without ADHD (Castellanos & Tannock, 2002; Douglas, 1999; Nigg, 2005; Sergeant, 2005). This result has been reported consistently with the two experimental paradigms most commonly used to study inhibition in ADHD: go/no-go tasks and stop signal reaction time tasks (a variant of the go/no-go task; Klein, Wendling, Huettner, Ruder, & Peper, 2006). Slowness and/or marked variability in ADHD have also been reported in other experimental tasks involving inhibitory processes (investigated with saccade tasks; Klein, Raschke, & Brandenbusch, 2003; Munoz, Armstrong, Hampton, & Moore, 2003), stimuli conflict (with flanker tasks; Drechsler, Brandeis, Foldenyi, Imhof, & Steinhausen, 2005; Ridderinkhof, Scheres, Oosterlaan, & Sergeant, 2005), alertness and visuospatial orienting (with Posner paradigms; Drechsler et al., 2005, Huang-Pollock & Nigg, 2003), visuospatial discrimination (with choice tasks; Leth-Steensen, Elbaz, & Douglas, 2000; Piek et al., 2004), and Continuous Performance Test (CPT, testing sustained attention; Weyandt, Mitzlaff, & Thomas, 2002). Recently, several authors have suggested that this response variability could be a unitary impairment in ADHD (Castellanos, Sonuga-Barke, Milham, & Tannock 2006; Epstein et al., 2003; Klein et al., 2006; Russell et al., 2006). To date, however, few studies have addressed the issue of response time and variability in the three ADHD subtypes, and the available results appear to be contradictory (depending on the method used). In studies comparing the three ADHD subtypes with children without ADHD performing a go/no-go or tapping task, slowness and more marked variability were both demonstrated in the inattentive and combined forms, whereas mean RT (MRT) and intraindividual standard deviation of RT (ISD) appeared to be relatively normal in the hyperactive/impulsive form (Chhabildas, Pennington, & Willcutt, 2001; Pitcher, Piek, & Barrett, 2002). The normal speed and variability reported during experimental tasks in the hyperactive/impulsive form is in contradiction with the clinical impression that children with ADHD-HI make many inadequate, rapid, impulsive responses both in everyday situations and on experimental tasks. Furthermore, in a large sample of children performing a go/no-go task, Epstein et al. (2003) showed that the ISD was nonspecifically related to all ADHD symptoms defined by DSM-IV (i.e., inattention but also hyperactivity and impulsivity), whereas the MRT was specifically related to hyperactivity. A similar correlation linking RT and inattention has also been reported in children with ADHD performing a choice reaction time task with visuospatial stimuli (Piek et al., 2004), but hyperactivity and impulsivity were not evaluated in this study. According to Epstein et al. (2003),

MRT and ISD measure different components of response time, despite being highly correlated (0.86 in this study). The authors suggested that ADHD symptoms are related to failure to adopt a consistent response strategy rather than an overall attenuation in response time. The fact that RT variability appeared to be linked with each ADHD symptom (including hyperactivity/impulsivity) is surprising, given the lack of evidence of abnormal mean response times in children with ADHD-HI performing experimental tasks. However, MRT and ISD may not be sufficiently sensitive indicators to reveal possible abnormal response times in children with ADHD-HI. Recently, two studies used the distributional analysis approach to study RT in ADHD. This consisted of calculating the frequency of responses per time interval or by fitting trial-by-trial RT data to an ex-Gaussian distribution to analyze speed and variability with a single global parameter (for a theoretical presentation of the exGaussian distribution, see Luce, 1986). Typically, the distribution of responses as function of time starts with an early normal component during which the number of responses increases rapidly up to a point (the peak of response frequency) at which the number of responses decreases abruptly. This normal component is followed by a late exponential component (tail) during which the response frequency decreases slightly over time until extinction of responses. In children with ADHD-C performing a four-choice task, Leth-Steensen et al. (2000) showed that the response distribution curve was flattened with a delayed frequency peak and an extended slow tail compared to children without ADHD. In children with ADHD performing a go/no-go CPT, Hervey et al. (2006) also found a flatter response distribution curve and an extended slow tail compared to children without ADHD. However, they reported that responses peaked earlier in children with ADHD than in children without ADHD. The fact that the peak frequency was faster in children with ADHD than in healthy children could reflect the fact that the go/no-go task induces more impulsive responses than the choice task in children with ADHD. This result could also be because of the presence of 12 ADHD-HI subjects in the ADHD group (comprising 26 children with ADHD-IA and children with 27 ADHD-C). Thus, children with ADHD present faster RT and less RT variability on the normal component of the frequency curve than children without ADHD. However, these children with ADHD presented longer MRT and more variable ISD than children without ADHD. These results indicate that distributional analysis measures additional components of responses compared to overall MRT and ISD indicators. They show that in certain

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68 Journal of Attention Disorders

circumstances, in this case a go/no-go task, children with ADHD could commit many impulsive responses (as reflected by the early peak frequency) and may respond very slowly at other moments of the task (as reflected by the extended slow tail).

Method
Participants
Groups were matched by age and gender to exclude the impact of these two factors, which are known to strongly influence RT and which may therefore influence RT distribution (for an example of the impact of age and gender on mean RT and RT variability on a large sample of children performing a CPT, see Conners, 1994). The ADHD groups were composed of children recruited from the outpatient of the regional center for learning disabilities at the Amiens University Hospital. ADHD was assessed according to the DSM-IV (American Psychiatric Association, 1994) with several instruments: SNAP IV short form questionnaires for parents and teacher (Pelham, Fabiano, & Massetty, 2005); semistructured interview with the child and his or her parents; ADHD rating scale (Dpfner et al., 2006; DuPaul, Power, Anastopoulos, & Reid, 1998). Neuropsychologic assessment was systematically performed and included the Kaufman Assessment Battery for Children (K-ABC; Kaufman & Kaufman, 1983) and/or the WISC-III. The K-ABC is a widely accepted test to assess cognitive function in children aged 4 to 12 years. In ADHD, the sequential scale score is often low, whereas the simultaneous scale score is normal (Robitaille, Everett, & Thomas, 1990). The exclusion criteria were as follows: a history of neurologic or psychiatric disorders other than ADHD, depression and/or generalized anxiety, sensorimotor deficits and a low IQ (WISC-III full scale score 80 or K-ABC simultaneous scale score 80). Children without ADHD attended regular school classes and showed normal levels of academic achievement. The following exclusion criteria were applied: learning difficulties or behavioral disorders, a history of behavioral, neurologic or psychiatric disorders, psychotropic medication, sensorimotor deficits or learning difficulties. The childrens parents received comprehensive information about the study and its objectives and the study was approved by the local ethics committee. Children were included in the HI subtype when they presented six or more hyperactive/impulsive symptoms and three or less inattentive symptoms. Children were included in the IA subtype when they presented six or more inattentive symptoms and three or less hyperactive/impulsive symptoms. Children were included in the C subtype when they presented six or more hyperactive/ impulsive symptoms and six or more inattentive symptoms. Four age- and gender-matched groups of 16 children aged 7 to 13 years were constituted: ADHD-IA, ADHD-HI, ADHD-C, and non-ADHD groups (for demographic and

Present Study
The objective of the present study was to investigate RT profiles in an attentional capture task in the three ADHD subtypes. The children had to make a motor response to spatial targets in the presence of moving stimuli that could potentially distract them from the target. In experimental tasks involving reproduction of time intervals or detection of visual targets in the presence of visual or sound distractors, abnormally high distractibility has been reported in ADHD (Barkley, Koplowitz, Anderson, & McMurray. 1997; Gumenyuk et al., 2005) and in each ADHD subtype (Keage et al., 2006; Leung & Connolly, 1996; Van der Meere & Sergeant, 1988). We therefore hypothesized that the moving distractor should have a greater impact (by slowing responses) in all children with ADHD compared to children without ADHD. In the few studies devoted to the three ADHD subtypes, abnormal longer MRT and more variable ISD have been reported in ADHD-IA and ADHD-C subtypes, whereas MRT and ISD were both relatively normal in the ADHD-HI subtype (Aase, Meyer, & Sagvolden, 2006; Chhabildas et al., 2001). We also hypothesized that MRT and ISD should be abnormally higher in children with ADHD-IA and ADHD-C than in children with ADHD-HI and children without ADHD. An abnormally higher error rate has also been reported in these studies for ADHD-HI and ADHD-C subtypes but not for the ADHD-IA subtype. Error rates should therefore be abnormally higher in children with ADHD-HI and ADHD-C than in children with ADHD-IA and children without ADHD. In a sample of children with ADHD-C performing a visual choice task, Leth-Steensen et al. (2000) showed that the RT distribution curve was flattened with a delayed peak frequency and an extended slow tail compared to children without ADHD. We therefore hypothesized that on a visual choice task, children with ADHD-C and ADHD-IAthose presenting inattentive symptoms should present a fairly similar RT-distribution curve to those reported by Leth-Steensen et al. (2000). In children with ADHD-HI, we hypothesized that impulsivity should lead them to commit many rapid impulsive responses. Consequently, we predicted that the response frequency should peak more rapidly in children with ADHD-HI than in children without ADHD.

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Patrick, Laurent / Response Time Distribution in ADHD Subtypes 69

Table 1 Demographic Data for ADHD-HI, ADHD-IA, ADHD-C and Non-ADHD Groups
Demographic data Ethnicity Group ADHD-IA ADHD-HI ADHD-C non-ADHD N 16 16 16 16 Mean age (SD) 10.33 (1.92) 10.33 (1.87) 10.38 (1.56) 10.36 (1.56) Gender 4 F / 12 M 4 F / 12 M 4 F / 12 M 4 F / 12 M White 15 14 13 15 North African 1 1 3 1 African 0 1 0 0 Drug naive 10 11 8 16

Note: F = female; M = male.

Table 2 Psychometric Data for ADHD-HI, ADHD-IA and ADHD-C Groups

Psychometric data K-ABC Group ADHD-IA ADHD-HI ADHD-C all ADHD Sequential scale (SD) 86.3 (9.1) 86.1 (9.4) 84.0 (12.1) 85.4 (10.0) Simultaneous scale (SD) 98.6 (12.0) 91.3 (6.7) 96.9 (8.1) 95.6 (9.3) N 8 8 9 25 Verbal scale (SD) 96.1 (16.3) 99.1 (21.0) 91.9 (7.3) 95.8 (15.9) WISC-III Performance scale (SD) 96.4 (12.1) 93.6 (14.4) 90.9 (10.0) 93.6 (12.1) N 11 12 11 34

Note: K-ABC = Kaufman Assessment Battery for Children; WISC-III = Wechsler Adult Intelligence ScaleIII. N indicates the number of children assessed by the KABC and/or WISC-III.

psychometric data, see Table 1 and Table 2, respectively). All children diagnosed as having ADHD were evaluated prior to treatment and/or during an off-treatment period. Treatment was stopped 48 hours before the experimental session for medicated children (the number of drug naive children is shown in Table 1).

Stimuli, Apparatus and Procedure

The attentional capture task consisted of locating a target displayed above or below a central fixation mark while attempting to ignore the motion jitter of an irrelevant lateral disk (the distractor). Because moving stimuli are highly effective in capturing attention (Abrams & Christ, 2003, 2005; Franconeri & Simons, 2003; Theeuwes, 1994), the motion jitter was expected to attract attention in a reflexive-automatic manner. Attentional capture involves the simultaneous operation of two distinct mechanisms. The first (goal-driven) process focuses attention on the location of the target square, whereas the second (stimulus-driven) draws attention automatically towards the disk vibration and is expected to slow down the target location processes.

Participants were seated 50 cm in front of a 17 in. color screen. Children responded via a computer-interfaced, two-key box placed directly and vertically in front of them. The software was written by P. Despretz (LNFP UMR CNRS 8160 Lille University Medical Center). A black cross was displayed at the center of the screen and served as a fixation mark. Two permanently displayed red disks (subtending a visual angle of 2 degrees) were centered 4 degrees left and right of the fixation mark at a viewing distance of 60 cm. The target was a black square (subtending a visual angle of 2 degrees) displayed 4 degrees above or below the fixation mark. The task consisted of locating the target (top vs. bottom) by pressing the appropriate response key. The target appeared 500 ms after the fixation mark and remained on the screen for 1500 ms or until a response was made. In half of the trials, one of the distractors moved abruptly (horizontal motion jitter) for 34 ms as the target appeared (speed: 14.7 degrees per second). Children were instructed to fixate the central marker, ignore the disks, and concentrate only on the spatial location of the target square. They were asked to designate the location of the square as accurately and as quickly as possible. Responses were

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70 Journal of Attention Disorders

given by the right and left thumbs, which were positioned on the top and bottom response keys, respectively. The experiment involved 100 trials (25 with distractor motion on the left, 25 with distractor motion on the right, and 50 with no distractor motion, presented in random order). The entire session lasted about 6 minutes.

Analytical Design
All RTs below 100 ms were excluded from subsequent analysis. A cut-off of 100ms is typically applied in experimental tasks to exclude anticipatory responses (for more details, see Hervey et al., 2006). The percentage error and overall parameters for mean RT (MRT) and intraindividual standard deviation of RT (ISD) were calculated. As mentioned above, MRT and ISD are highly correlated. To take into account each individuals overall response speed, an additional variability parameter was calculated. The intraindividual coefficient of variation (ICV) was defined as ISD divided by MRT. The ICV parameter has been previously used to investigate response variability in ADHD but never in studies devoted to ADHD subtypes (Klein et al., 2006). Four separate analyses of variance (ANOVAs) were performed on the percentage error, MRT, ISD and ICV, respectively, with distractor (control / distractor trials) and target position (top/bottom) as within-group factors and ADHD group (ADHD-HI/ ADHD-IA/ADHD-C/ non-ADHD) as between-group factor for each ANOVA. A Newman-Keuls test was used for post hoc comparisons performed on percentage error, MRT, ISD and ICV. The first ANOVA run on errors tested the hypothesis that hyperactive/impulsive symptoms should be associated with an abnormally high error rate. A significant mean effect of group was expected and post hoc analysis should demonstrate a significantly higher error rate in the ADHD-HI and ADHD-C groups than in the ADHD-IA and non-ADHD groups. The second ANOVA run on MRT tested the hypothesis that children with inattentive symptoms should respond more slowly than children in the ADHD-HI and non-ADHD groups. A significant group effect was expected and post hoc analysis should demonstrate significantly longer MRT in the ADHD-IA and ADHD-C groups than in the ADHD-HI and nonADHD groups. Distractibility should be higher in the ADHD group than in the control group. The second ANOVA should demonstrate a significant interaction between distractor and group. The post hoc analysis should demonstrate a higher distractor effect in the ADHD-HI, ADHD-C and ADHD-HI groups than in the non-ADHD group. The third ANOVA run on ISD tested the hypothesis that the ADHD-IA and ADHD-C groups should respond with greater variability than the ADHD-HI and

non-ADHD groups (within- and between-group factors are indicated above). A significant group effect was expected. The post hoc analysis should demonstrate significantly higher ISD in the ADHD-IA and ADHD-C groups than in the ADHD-HI and non-ADHD groups. We hypothesized that the variability of RT should reveal an abnormally high variability in each ADHD subtype when related to the mean intraindividual RT. The fourth ANOVA run on ICV tested the hypothesis that each ADHD group should exhibit a greater variability related to individual response time than non-ADHD groups (within- and between-group factors are indicated above). A significant group effect was expected. The post hoc analysis should demonstrate significantly higher ISD in the ADHD-HI, ADHD-IA and ADHD-C groups than in the non-ADHD group. The frequency of correct responses (Hit-RT) was calculated for each 100 ms RT interval from 101 ms to 1500 ms by dividing the number of correct responses made in each RT interval by the total number of responses made during the task. For example, the Hit-RT frequency in the interval (300 ms < RT 400 ms) was the number of correct responses longer than 300 ms and shorter or equal to 400 ms divided by the total number of responses. The RT intervals are expressed in the text by the RT value in the center of the interval (I-350, in the example given above). An ANOVA was performed on Hit-RT frequencies by taking into account RT-interval (from I-150 to I-1450) as a withingroup factor and ADHD group (ADHD-HI/ ADHD-IA/ ADHD-C/non-ADHD) as a between-group factor. The Bonferroni test was used for post hoc comparisons of the Hit-RT frequency distribution to reduce the likelihood of a family-wise Type I error. The fifth ANOVA run on Hit-RT frequencies tested the hypothesis that children with ADHD-HI should present a fast go mode response, whereas children with ADHD-IA and ADHD-C should present a slow mode response compared with children without ADHD. The post hoc analysis should demonstrate more responses in the first part of the RT distribution and fewer responses in the last part of the RT distribution in the ADHD-HI group than in the control group. It should also demonstrate fewer responses in the first part of the RT distribution and more responses in the last part of the RT distribution in the ADHD-IA and ADHD-C groups than in the control group.

Results
Overall Performance for Errors and Response Time
Errors. The ANOVA on errors evidenced a marked group effect, F(3,60) = 6.8, p < .00052. The percentage

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Patrick, Laurent / Response Time Distribution in ADHD Subtypes 71

error rate in the ADHD-HI (12.7%) and ADHD-C (14.7%) groups was significantly higher than in the ADHD-IA group (5.9%) and non-ADHD group (4.1%; see the appendix for the post hoc test results). No effect of the distractor, F(1,60) = 0.2, p < .66, or target position, F(1,60) = 1.7, p < .17, was observed on the error rate. MRT. The ANOVA on MRT revealed a significant effect of the group factor, F(3,60) = 6.7, p < .00057. Responses were significantly slower in the ADHD-IA (551 ms) and ADHD-C (541 ms; ISD) groups than in the ADHD-HI (426 ms) and non-ADHD (421 ms) groups (see the appendix for the post hoc test results). As expected, the motion jitter distractor slowed overall RTs. The ANOVA indicated a simple effect of distractor on MRT, F(1,60) = 11.3, p < .0014, with no significant group effect. Compared with control trials, distractor trials slowed responses in the ADHD-IA (+17 ms), ADHD-C (+23 ms) and control (+18 ms) groups but accelerated responses in the ADHD-HI group (3 ms). Planned comparisons indicated that the differences between distractor and control trials were significant in the ADHD-IA (p < .041), ADHD-C (p < .0064) and non-ADHD (p < .033) groups but were not significant in the ADHD-HI group. In contrast to previous reports in the ADHD literature, the distractor did not have a greater impact on MRT in children with ADHD than in children without ADHD. Moreover, it can even be suggested that children with ADHD-HI were less sensitive to distractors than children in the other groups (including the nonADHD group). No effect of target position on MRT was observed, F(1,60) = 0.1, p < .74. ISD. The ANOVA on ISD revealed a significant effect of the group factor, F(3,60) = 11.2, p < .000006. Responses were significantly more variable in the ADHD-IA (184 ms) and ADHD-C (190 ms) groups than in the ADHD-HI (137 ms) and non-ADHD (ISD: 104 ms) groups (see the appendix for the post hoc test results). No effect of the distractor, F(1,60) = 0.2, p < .69, or target position was observed on ISD, F(1,60) = 1.1, p < .31. ICV. The ANOVA on ICV evidenced a marked group effect, F(3,60) = 10.7, p < .00001. The ICV was significantly higher in the ADHD-HI (0.312), ADHD-IA (0.335), and ADHD-C (0.349) groups than in the nonADHD group (0.246; see the appendix for the post hoc test results). Despite the fact that the MRT and ISD analyses failed to demonstrate any difference in RT between the ADHD-HI group and the non-ADHD group, analysis of ICV showed that RT variability was greater in all ADHD subtypes than in the non-ADHD group. This result demonstrates that when individual response time

were taken into account, RTs were more variable in each the ADHD subtype group than in the non-ADHD group. No effect of the distractor, F(1,60) = 2.4, p < .13, or target position was observed on ICV, F(1,60) = 1.3, p < .25.

Response Time Distribution

Examination of the Hit-RT frequency distribution indicated that ADHD-HI children made more fast responses and fewer slow responses than control children, whereas ADHD-IA and ADHD-C made fewer fast responses and more slow responses than children without ADHD (see Figure 1). The distribution curve shapes were fairly similar for children with ADHD-IA and ADHD-C, although the ADHD-C curve appeared to be flatter than the ADHD-IA curve. The ANOVA performed on the Hit-RT frequency distribution indicated a Marked Group RT-Interval interaction, F(39,780) = 6.3, p < .000001. The Bonferroni post hoc analysis confirmed that the ADHD-HI and non-ADHD groups differed in terms of their response distribution curves. In the ADHD-HI group, response frequencies were significantly higher for I-250 (p < .000001) and lower from I-450 to I-550 than in the non-ADHD group (p < .000001 for both RT-intervals), whereas no significant difference was observed for the other RT-intervals. In the ADHD-IA group, frequencies were significantly lower from I-250 to I-450 (p < .000001 for all RT-intervals) and significantly higher for I-550 and I-850 than in the non-ADHD group (with p never less than .0047), whereas no significant difference was observed for the other RT-intervals. In the ADHD-C group, frequencies were significantly lower from I-250 to I-450 (p < .000001 for all of these RT-intervals) and significantly higher for I-650 and I-750 than in the non-ADHD group (p < .000001 for all of these RT-intervals); no significant difference was observed for the other RT-intervals. Except for I-450, where the Hit-RT frequency curve reached a slightly higher peak in the ADHD-IA group than in the ADHD-C group (p < .04), no significant difference were observed for the other RT intervals.

Discussion
As expected, responses to the target were slowed in the presence of nearby motion jitter, indicating that motion distracted the processes aimed at locating the target in space and/or generating choice and motor responses. However, no significant difference was observed between the ADHD subtype groups and the non-ADHD group in terms of the effect of the distractor

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72 Journal of Attention Disorders

Figure 1 Hit-RT Frequencies by Group (ADHD-HI/ADHD-IA/ADHD-C/non-ADHD) as a Function of RT Interval (From I-150 to I-1450)

on RT. Motion jitter had a similar impact on RT in children with ADHD-IA, ADHD-C and children without ADHD and appeared to have a lesser impact on RT in children with ADHD-HI than in children without ADHD. This result is in contradiction with previous reports in which more marked distractibility was observed in all ADHD subtypes compared with children without ADHD (Keage et al., 2006; Leung & Connolly, 1996; Van der Meere & Sergeant, 1988). One possible explanation is that children with ADHD and those without ADHD differ in terms of their sensitivity to motion jitter, but the sample size of the present study may have been too small to demonstrate significant intergroup differences in distractibility. The results concerning successful spatial location of the target indicate that children with ADHD-IA did not differ from children without ADHD in terms of error rate, whereas children with either ADHD-C or ADHD-HI clearly gave more false responses than children without ADHD. Similar results have been previously reported for a range of experimental tasks. Impairments in ADHD-C and ADHD-HI (associated with little or no impairment in ADHD-IA children) have been demonstrated for

omission in the CPT (Chhabildas et al., 2001), for error rate in a learning visuospatial task (Aase, Meyer, & Sagvolden, 2006), for incorrect eye movements in the anti-saccade task (ODriscoll et al., 2005), and for error rate in the flanker task (Oberlin, Alford, & Marrocco, 2005). However, it should be noted that these last two studies did not include any ADHD-HI children. Examination of MRT and ISD showed that responses were slower and more variable in ADHD-IA and ADHD-C children compared to either ADHD-HI or children without ADHD. Similar results with the same parameters have been reported in ADHD subtypes in children performing the CPT or a tapping task (Chhabildas et al., 2001; Pitcher et al., 2002). However, this result cannot be generalized to all experimental tasks. For example, in a flanker task, slower and more variable responses have been demonstrated in children with ADHD-C but not in children with ADHD-IA, compared to children without ADHD (Oberlin et al., 2005). However, the relative variability estimated by ICV was clearly higher in each ADHD subtype (including ADHD-HI) than in children without ADHD. This result suggests that responses in each ADHD subtype were abnormally variable when

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Patrick, Laurent / Response Time Distribution in ADHD Subtypes 73

normalized to their respective overall speeds and supports the hypothesis proposed by Epstein et al. (2003): MRT and ISD do not measure the same components of the RT, despite the fact that the two variables are highly correlated. This finding is in agreement with the hypothesis formulated by Epstein et al. (2003), Klein et al. (2006), and Russell et al. (2006) that response variability could be a unitary cognitive impairment in ADHD. In children performing a flanker task, Castellanos et al. (2005) reported that reaction time variability in ADHD differed quantitatively from children without ADHD, particularly at a modal frequency of around 0.05 Hz. In this article, the authors proposed that these transient but relatively frequent lapses in attention (2-4 times per minute) underlie behavioral symptoms such as difficulty sustaining attention, forgetfulness, disorganization, and careless errors in ADHD. Examination of the RT distribution provides a more detailed view of how children with ADHD respond as function of subtype. The RTs recorded in both the ADHD-C and ADHD-IA groups were dramatically slower at the end of the RT-distribution than those recorded in the non-ADHD group. Our results also showed that the RT distribution in the ADHD-HI group was clearly different from those observed in the other two ADHD groups and also differed from those observed in the non-ADHD group. The RT-distribution curve was shifted to the left in the children with ADHD-HI, compared with children without ADHD. Children with ADHD-HI responded more frequently in the fast part of the RT distribution but less frequently at the slow end than children without ADHD and children with ADHD with attentional deficits (ADHD-IA and ADHD-C subtypes). The long, slow tail of the RT distribution found in the ADHD-C and ADHD-IA groups is consistent with results reported previously by Leth-Steensen et al. (2000) for a group of 17 children with ADHD-C (aged from 9 to 13 years) performing a four-choice reaction time task. In the study by Hervey et al. (2006), children with ADHD (M = 10.7 years) gave more responses during the early fast part and slow end of the RT distribution than children without ADHD (i.e., the ADHD curve was flattened and extended in both directions along the RT axis, compared with the curve of the non-ADHD group). The comparison between our results and those reported by Hervey et al. and Leth-Steensen et al. is difficult because the experimental tasks and populations were different. It can be suggested that the more frequent responses at the early fast part of the distribution in the study by Hervey et al. may have been because of the presence of 12 ADHD-HI subjects in the ADHD group (with 26 children with ADHD-IA and 27 children with ADHD-C). It should be noted that ADHD subtypes were

not analyzed in this study. It can also be suggested that the distribution of responses in ADHD depends on whether when the task involves inhibition of a prepotent response (go/no-go in Hervey et al., 2006) or visuospatial location (multiple choice in the present study and in Leth-Steensen et al., 2000). The present results suggest that (a) the distributional approach allows demonstration of RT anomalies in each ADHD subtype on the capture task and (b) the direction of the skewness in the RT distribution clearly distinguishes ADHD with predominant hyperactivity/impulsivity symptoms from both ADHD with inattention symptoms and children without ADHD.

Contribution to the Question of Subtypes in ADHD

The debate concerning subtypes is complicated by the fact that subtype classifications often change over time in a given child (Lahe, et al., 2005). Longitudinal studies show that children meeting criteria for ADHD-HI around the age of 4 to 6 years rarely remain in this group but shift to ADHD-C in later years (Lahey et al., 2004, 2005). Lahey et al. (2005) proposed that ADHD-HI should be viewed as a milder form of ADHD-C that often exhibits sufficiently serious attention problems later in elementary school to meet the criteria for ADHD-C. However, they also stressed that young children who met criteria for ADHD-HI could likely shift to the combined subtype as increasing demands of school made their attention problems more evident. The present study showed that RT-distribution profiles differed very markedly between ADHD-HI and ADHD-C groups with an opposite direction compared to the non-ADHD group. Age was closely matched between children included in each group (see Table 1), excluding an impact of this factor on differences in performance between groups. The large amplitude of the differences observed in our sample of children with ADHD-HI and ADHD-C appear to contradict the concept that ADHD-HI could be a precursor, or milder form, of ADHD-C. This study does not resolve the issue of the validity of ADHD-HI subtypes raised by Milich et al. (2001), but our results at least suggest that children meeting DSM-IV (American Psychiatric Association, 1994) criteria for ADHD-HI present different types of cognitive impairment to those with ADHD-C in our sample. Several authors point out that ADHD-IA and ADHD-C groups differ in terms of several important dimensions other than the presence of hyperactive and impulsive symptoms (Derefinko et al., in press; Diamond, 2005; Milich et al. 2001), suggesting that ADHD-IA and ADHD-C could be two distinct disorders with different phenotypes and different underlying pathologies. These

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74 Journal of Attention Disorders

authors claim that ADHD-C is often associated with distractibility and inhibitory impairment, whereas ADHD-IA seems to be characterized by a sluggish cognitive tempo and core deficits for working memory (Derefinko et al., in press; Diamond, 2005; Solanto et al., 2006). In contrast, other authors have reported that ADHD-C and ADHD-IA groups both present sluggish cognitive tempo symptoms compared to those meeting criteria for ADHD-HI and non-ADHD (Hartman, Willcutt, Rhee, & Pennington, 2004). Similarly, little or no differences have been reported between ADHD-C and ADHD-IA groups for inhibition and response time on the go/no-go CPT (Riccio et al., 2006) and in many electroencephalographic studies (Clarke, Barry, McCarthy, Selikowitz, & Brown, 2001, 2002; Monastra et al., 1999; Monastra, Lubar, & Linden, 2001). These studies consistently show a pattern of electrophysiological slowing in both ADHD-IA and ADHDC groups compared to the non-ADHD group. When subtle differences were observed between groups, the slowness of electrophysiological indicators was more pronounced in ADHD-C than in ADHD-IA group (during eyes closed in Clarke et al., 2001; during drawing but not for eyes fixing, reading, or listening in Monastra et al., 1999). What is interesting is that Monastra et al. (2001) failed to demonstrate any electrophysiological differences between children with ADHD-C or ADHD-IA when performing the go/no-go task despite more severe inhibition in ADHD-C than in ADHD-IA (this study also did not find any difference for drawing, eyes fixing, reading or listening). The present results indicated that errors in locating the target were more frequent in the ADHD-C group than in the ADHD-IA group, whereas their response time profiles and their sensitivity to the moving distractor were fairly similar. As reported in several previous studies, the present study indicated that ADHD-C and ADHD-IA groups presented more similarities than differences. Finally, the results observed in this sample of children argue against the concept that ADHD-IA and ADHD-C could be two distinct disorders (Derefinko et al., in press; Diamond, 2005; Milich et al. 2001). These results appear to be more consistent with the idea that ADHD-IA constitutes a subtype of ADHD without hyperactivity/impulsivity, or at least a milder form of ADHD-C. The present findings do not resolve the controversy concerning ADHD subtypes. Further research is necessary to clarify this issue by strictly controlling for age and classification and by comparing the same sample of children in various experimental tasks.

controversial. Recently, a more complex model has been proposed by Castellanos et al. (2006) in which inattention may be associated with cool executive function deficits (such as inhibition dysfunction and slowness), whereas hyperactivity/impulsivity may be associated with hot executive function deficits (such as delay aversion impairment; Kuntsi, Oosterlaan, & Stevenson, 2001; Sonuga-Barke, 2003). The direction of the skewness observed in our study during a visual decision task appears to fit well with the above-mentioned hot-cool executive function deficit hypothesis. In children with ADHD-HI, the combination of a left-ward skewness in the RT distribution (e.g., too many rapid responses) and a high error rate clearly reflects the impairment resulting from cognitive impulsivity. In contrast, the right-ward skewness (e.g., too many responses at the slow end of the distribution) observed in children with ADHD-IA and ADHD-C reflects the impairment resulting from inattention and slowness. Lastly, in children with ADHD-C, who suffer from both inattention and cognitive impulsivity, the right-ward skewness is associated with a high error rate (see Figure 2 for a diagrammatic representation of this hypothesis). Castellanos and Tannock (2002) suggest that inattention, and not hyperactivity/impulsivity, is the strongest predictor of slowed response. The present findings in children with ADHD-IA or ADHD-C support this proposition. Moreover, our results in children with ADHD-HI suggest that hyperactivity/ impulsivity (and not inattention) could be a strong predictor of left-ward skewness.

Limitations and Future Directions

The model described above could be restricted to experimental tasks involving a multiple choice decision and/or visuospatial task, as the results reported using motor function tasks are more contrasted: When slowness and greater variability have been found to be confined to inattentive and combined forms (Pitcher et al., 2002), other studies have reported that children with ADHD-C appeared to be significantly more impaired when motor speed was required and showed greater error rate variability than children with ADHD-IA and ADHD-HI (Meyer & Sagvolden, 2006; Mullins, Bellgrove, Gill, & Robertson, 2005). In children performing the stop signal task, abnormal inhibition delays have been reported not only in the inattentive and combined forms but also in the hyperactive/impulsive form (Schachar et al. 2004). Several studies have demonstrated that children with ADHD could shift from one subtype to another in the course of their development. Four- to six-year-old children with ADHD-HI frequently shift to ADHD-C

Hot and Cool Deficits

The idea that all ADHD subtypes could be caused by impairment of a single, specific brain function is highly

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Patrick, Laurent / Response Time Distribution in ADHD Subtypes 75

Figure 2 Summary of the Relationships Between Performance Levels in the Capture Task (RT-Distribution Skewness and Error Rates) and Cognitive Impairments (Cognitive Impulsivity and Inattention) in the Three ADHD Subtypes (ADHD-HI/ADHD-IA/ADHD-C)

during the first level of elementary school, and those diagnosed with ADHD-C shift to ADHD-IA during middle or high school (Lahey et al., 2004, 2005; Wolraich et al., 2005). In the present study, all children were at elementary or higher school level (children were aged from 7 to 13 years). This limits the risk of underestimating inattentive symptoms in younger children, resulting

in a false diagnosis of ADHD-HI in children actually presenting the combined subtype. As shown for ADHDHI, the initial ADHD-C classification can change over time in a given child. Some children classified as ADHD-C around the age of 4 to 6 years shift to ADHD-IA during middle school or later (Lahey et al., 2004, 2005; Wolraich et al., 2005). Initial hyperactivity/impulsivity symptoms could decline spontaneously during late childhood and adolescence or could be underestimated as they appear less marked during adolescence compared with children without ADHD (Wolraich et al., 2005). It is more difficult to avoid a false diagnosis of ADHD-IA in children presenting the combined subtype. This risk may have concerned some, but not all of the older children of our sample. The age range studied here was limited to children 7 to 13 years old, and the small sample size may limit generalization of the present results to the population of ADHD. In line with previous studies by Leth-Steensen et al. (2000) and Hervey et al. (2006), the present study suggests that the distributional approach is a powerful tool for studying response times in ADHD subtypes, but further investigations with larger populations covering a broader age range and other experimental tasks are required to provide a better understanding of the link between neuropsychologic indicators and experimental parameters. Considering that ADHD subtype classifications often change over time, future studies will need to investigate stability of the RT-distribution profile in children followed longitudinally.

Appendix P values for Newman-Keuls Post Hoc Comparisons of Study Groups (ADHD-HI/ADHD-IA/ADHD-C/non-ADHD) For Errors, Mean RT (MRT), Intraindividual RT Standard Deviation (ISD), and Intraindividual Coefficient of Variation (ICV).
Group Non-ADHD ADHD-HI ADHD-IA ADHD-C Non-ADHD ADHD-HI ADHD-IA ADHD-C Non-ADHD ADHD-HI ADHD-IA ADHD-C Non-ADHD ADHD-HI ADHD-IA ADHD-C p .0086 ns .0019 ns .0075 .0083 ns .0002 .0002 .0014 .0002 .0002 p .0086 .0188 ns ns .0057 .0043 ns .0080 .0085 .0014 ns ns P ns .0188 .0074 .0075 .0057 ns .0002 .0080 Ns .0002 ns ns p .0019 ns .0074 .0083 .0043 ns .0002 .0085 ns .0002 ns ns Error (4.1 %) (12.7 %) (5.9 %) (14.7 %) (421 ms) (426 ms) (551 ms) (541 ms) (104 ms) (137 ms) (184 ms) (190 ms) (0.25) (0.31) (0.33) (0.35) MRT ISD ICV

Note: Values of p .05 are indicated by ns (nonsignificant).

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76 Journal of Attention Disorders

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Laurent Querne received his M.D. from the University of Caen Basse-Normandie France. He is currently a postdoctoral student at the Amiens University Medical Center. His research interests include developmental neuropsychology and ADHD. Patrick Berquin, M.D., Ph.D., is a clinical professor in pediatric neurology at Jules Verne University of Picardy France. He has authored several manuscripts on ADHD in children. He obtained his MD and PhD from Jules Verne University of Picardy and completed his residency training in Lille and Brussels. He also completed research training as visiting associate at the NIMH.

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