Timing and force control in boys with attention deficit hyperactivity disorder: Subtype differences and the effect of comorbid developmental coordination disorder
Introduction
Children with attention deficit hyperactivity disorder (ADHD) experience a persistent condition that can lead to life long problems. Diagnosis of ADHD requires identification of a specific number of symptoms from an inventory of persistent inattentive and/or hyperactive–impulsive behaviours that are inconsistent with their developmental level and are maladaptive (American Psychiatric Association, 1994). Characteristically, these children may be unable to plan ahead or complete tasks and may demonstrate increased levels of activity and/or impulsivity. Three distinct subtypes are identified in the most recent formulation of ADHD, namely, ADHD-predominantly inattentive (ADHD-PI), ADHD-hyperactive–impulsive (ADHD-HI) and ADHD-combined (ADHD-C) (American Psychiatric Association, 1994). The diagnostic criteria needed to meet either of the single diagnostic subtypes requires a child to have either six of nine inattention symptoms (ADHD-PI) or six of nine hyperactive–impulsive symptoms (ADHD-HI) but not reach the specified number of symptoms for the alternate diagnosis. To meet the ADHD combined type diagnosis (ADHD-C), a child must meet the criteria for both the inattention and hyperactive/impulsive symptoms.
The link between ADHD and motor coordination difficulties such as developmental coordination disorder (DCD) is well founded (e.g., Barkley, DuPaul, & McMurray, 1990; Hartsough & Lambert, 1985; Piek, Pitcher, & Hay, 1999). However, research examining the underlying motor functions of children with DSM-IV ADHD subtypes is limited, and findings to date are inconsistent. Although the most recent formulation of ADHD emphasises three distinct subtypes, earlier work (e.g., Hartsough & Lambert, 1985) has focused primarily on children with hyperactivity/impulsivity and is therefore more informative of DSM-IV ADHD subtypes with this type of symptomatology. To date, research specifying the severity and range of movement difficulties experienced by children with subtypes that include inattention has not been comprehensively documented.
The information processing approach has been used to investigate the underlying motor difficulties of both children with ADHD (van der Meere, 1996) and those with dysfunctional motor coordination (e.g., Wilson & McKenzie, 1998). The ‘input’ stage of information processing involves perceptual processes such as the registration, integration and interpretation of sensory information (Wilson & McKenzie, 1998). Perceptual processes in particular appear to be disrupted in children with DCD (e.g., Coleman, Piek, & Livesey, 2001; Wilson & McKenzie, 1998). Central processes are responsible for the response-selection stage, which involves decisions on the response required. Motor, or output processes involve the organisation and initiation of the appropriate response or motor program. It is this stage that has received considerable attention in the ADHD literature.
Children with ADHD are often found to be slow, inaccurate performers (Jennings, van der Molen, Pelham, Debski, & Hoza, 1997; Oosterlaan & Sergeant, 1996; Scheres, Oosterlaan, & Sergeant, 2001; van der Meere, 1996; van der Meere & Sergeant, 1988) where delayed motor processing is considered a core deficit (see also Sergeant & van der Meere, 1988; van der Meere, Vreeling, & Sergeant, 1992). These findings have led to the development of a motor output deficit hypothesis (Sergeant & van der Meere, 1988; van der Meere, 1996; van der Meere et al., 1992). In particular, children with hyperactivity have demonstrated greater reaction time (RT) variability in performance on various psychometric tasks than control children (Douglas, 1972; Jennings et al., 1997; van der Meere & Sergeant, 1988). However, as discussed by Rubia, Oosterlaan, Sergeant, Brandeis, and van Leeuwen (1998), RT outcomes and their variability require contextual analysis of associated task demands (i.e., cognitive, sensory and motor related demands). Thus, it is possible that observed outcomes may be less related to specific motor deficits than to difficulties with executive functions (e.g., attentional, memory) that are taxed by the test construction. From an information processing perspective, attention (i.e., the rate of information processing within the working memory system (Schiffrin and Schneider, 1977, cited in Sergeant & van der Meere, 1990)) assists the process of stimuli recognition, response selection and response organisation as compatible memory traces are accessed, selected and assimilated, and incompatible activities are attenuated (Keele, 1973).
Using primed and delayed RT tasks, output stage processing difficulties were again implicated for children with ADHD (Leung & Connolly, 1997). Yet, interestingly, a choice RT paradigm follow-up study with the same sample, whilst finding significant differences in RT, Movement Time (MT) and their variability as a function of task complexity (i.e., number, and position, of keys within the movement sequence), found no significant difference in motor organisation or motor execution (Leung & Connolly, 1998). However, this result may have been influenced by low power due to small group sizes and the authors agreed that cross-validation was necessary (Leung & Connolly, 1998). A factor restricting the applicability of these findings to DSM-IV ADHD is the omission of children without symptoms of hyperactivity–impulsivity (i.e., ADHD-PI). This factor arose due to the authors’ utilisation of ICD-10 criteria. Indeed, investigation of subtype variance with respect to RT is limited.
Simple finger tapping tests (e.g., number of taps completed within a specified time interval) have often been used within a battery of neuropsychological tests for children with ADHD in order to gauge motor speed (e.g., Seidman et al., 1995; Seidman, Faraone, Biederman, Weber, & Oulette, 1997). Slower tapping speed has been linked to inattentive symptomatology in community samples although some participants had comorbid hyperactive–impulsive and disruptive behaviours (McGee et al., 1985, McGee et al., 1987). Stevens, Stover, and Backus (1970) also report slower response rates and an inability to speed up when instructed to or when provided with an incentive. However, others report no significantly different performance to that of the controls (e.g., Gordon & Kantor, 1979; Seidman et al., 1995). Seidman and colleagues (e.g., Seidman et al., 1995; Seidman et al., 1997) failed to find any significant motor speed difference in children with varying comorbid combinations of learning difficulties, ADHD (DSM-III-R) and family history ADHD as compared to control children. These simpler tests of fine motor skills (i.e., simple tapping speed) do not seem to be as affected as the more complex motor sequences (Breen, 1989; Grodzinsky & Diamond, 1992; Mariani & Barkley, 1997).
Given the relationship between timing and force to the production of movement, there is surprisingly little in the ADHD literature on this aspect of functioning, with two exceptions. Pereira, Eliasson, and Forssberg (2000), using a grip-force technique, found that boys with ADHD (DSM-III-R) and motor performance difficulties displayed greater variability in force output and impaired sensory motor control than control children (Pereira et al., 2000). Boys with ADHD and no motor difficulties were found to have inconsistent force output more similar to the ADHD/motor impaired group than the control group. However, the grip-force task did discriminate the loci of dysfunction from “sensory information processing, the storage and retrieval of the memory representation, or the programming of the motor commands” (Pereira et al., 2000, p. 551). A study by Steger et al. (2001) examined neuromotor and attentional deficits in a group of 11 year old children with ADHD (DSM-III-R). Force was continuously monitored during both unilateral and bilateral RT tasks that required an “opposing pressure of thumb and index finger (precision grip)” response to the visual stimuli (Steger et al., 2001, p. 174). Children with ADHD were found to take longer to reach peak force (PF) and had more variability in their RT to force onset (Steger et al., 2001).
The aim of the current study was to utilise the information processing approach to derive understanding about the timing and force variables disrupted in each of the three ADHD subtypes. A sequential tapping task was used to analyse the timing of movement and its variability when task complexity was manipulated by requiring the previewed, accentuation of force on none, one or more taps within a five-tap sequence. Increasing the complexity of the task increases the cognitive load (Piek, Glencross, Barrett, & Love, 1993; Piek & Skinner, 1999). Earlier studies investigating timing in children with ADHD have often relied on tasks that have minimal motor related procedures and were often more visuo-spatially oriented (e.g., the visual search task of Sergeant & Scholten (1985a)). Leung and Connolly (1998) argued that “different processes are examined” in tasks that manipulate aspects such as event rate (e.g., van der Meere et al., 1992), whereas tasks that manipulate the sequence complexity are more reflective of the “organization and execution of serial movement” (p. 605). The task used in the current study was developed specifically to examine the organization and execution of movement sequences (e.g., Refer to Garcia-Colera & Semjen, 1988; Keele, Ivry, & Pokorny, 1987; Klapp & Wyatt, 1976; Piek & Glencross, 1993; Piek et al., 1993; Semjen & Garcia-Colera, 1986; Semjen, Garcia-Colera, & Requin, 1984; Wing, Keele, & Margolin, 1984), and has been successfully used on children with DCD who were shown to have timing related impairment (Piek & Skinner, 1999). The technique enables the measurement of RT, inter-tap interval (ITI) relating to overall movement speed, and PF.
The participant pool was distinguished in two distinct ways to address two separate issues. The first analysis involved examining four groups of boys, a comparison group and each of the three subtypes of ADHD as defined by the DSM-IV. It was hypothesised that boys in the ADHD groups would have longer RTs for each tapping force condition than boys in the comparison group (e.g., Lorys, Hynd, & Lahey, 1990; Oosterlaan & Sergeant, 1996; Ullman, Barkley, & Brown, 1978; Zahn, Kruesi, & Rapoport, 1991). They would also show significantly different PF output for each tapping force condition than the boys in the comparison group (e.g., Pereira et al., 2000), and would have significantly longer ITIs than the comparison group within the complex force (i.e., accentuation) conditions (e.g., Sergeant & Scholten, 1985a; Sheppard, Bradshaw, Georgiou, Bradshaw, & Lee, 2000; van der Meere et al., 1992). Finally, it was expected that each of the ADHD subtypes would have significantly greater timing and force variability as demonstrated by their mean RT, mean PF and mean ITI when compared to the comparison group (e.g., Leung & Connolly, 1994; Pereira et al., 2000; Schachar, Tannock, & Logan, 1993; Sergeant & Scholten, 1985a).
The second approach involved the comparison of boys with a single diagnosis of ADHD, with those who have a dual diagnosis of ADHD and DCD. A third, control, group was also included. This was designed to determine the comparative degree of difficulty for children with a single compared with a dual diagnosis, and to determine whether deficits for a single or dual diagnosis also differ in terms of the processes disrupted. It was expected that boys with comorbid ADHD/DCD would have significantly poorer performance on each experimental measure than either the ADHD only or control groups. Given that a disruption in input processes has been identified for children with DCD (e.g., Wilson & McKenzie, 1998), and output processes have been linked to children with ADHD (e.g., Sergeant & van der Meere, 1988), it would be expected that different processes would be identified for children with a single versus a dual diagnosis. This provides insight into the suitability of the definitional criteria detailed within the DSM-IV ADHD section with respect to the lack of formal recognition of the potential for comorbid DCD (American Psychiatric Association, 1994).
Section snippets
Participants
The sample for the current study was a community sample derived from main stream primary schools, across a broad spectrum of socio-economic localities, within the Perth metropolitan area.
Reaction time
Fig. 2 shows the group mean logarithmic RTs plotted as a function of force condition. The mixed design ANOVA for the RT data found both a statistically nonsignificant two-way interaction between Group and Force, F(6,272)<1, and main effect for Force, F(2,272)=2.38, p=0.094. A statistically significant main effect was found for Group, F(3,136)=2.89, p=0.038. This was followed by planned contrasts across the marginal means for the Group factor. The ADHD-PI and ADHD-C groups were
ADHD comparisons with or without comorbid DCD
For these comparisons, the same variables were recorded but the criteria for group allocation was different. In this analysis, participants were allocated into one of three groups according to the presence or absence of ADHD and/or DCD.
General discussion
This paper investigated timing and force dysfunction within boys with ADHD from two perspectives. The first perspective, ADHD subtype analysis, may be viewed as the typical approach to the investigation of cognitive and timing abilities for children with inattentive or hyperactive/impulsive symptoms. The outcome from the current study indicated that the ADHD-PI and ADHD-C subtypes experience significant underlying timing and force dysfunction as compared to the comparison boys. On face value,
Acknowledgements
This research was principally supported by a scholarship from The Women’s Service Guild (WSG) of WA Trust and a private research grant provided by Mr Ian and Mrs Jean Hutcheson to the first author. We wish to thank the participants, their parents and the participating schools for their support of this research. Also thanks to Motohide Miyahara, Peter Wilson and Natalie Gasson for their valuable comments on this paper.
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