J Clin Exp Neuropsychol. 2016;38(2):183-96. doi: 10.1080/13803395.2015.1094028.
Evidence of motor-control difficulties in children with attention deficit hyperactivity disorder, explored through a hierarchical motor-systems perspective.
- 1Department of Educational Psychology and Leadership Studies , University of Victoria , Victoria , BC , Canada.
- 2Department of Psychology , University of Victoria , Victoria , BC , Canada.
Attention deficit hyperactivity disorder (ADHD) may reflect a disorder of neural systems that regulate motor control. The current study investigates motor dysfunction in children with ADHD using a hierarchical motor-systems perspective where frontal-striatal/”medial” brain systems are viewed as regulating parietal/”lateral” brain systems in a top down manner, to inhibit automatic environmentally driven responses in favor of goal-directed behavior. It was hypothesized that due to frontal-striatal hypoactivation, children with ADHD would have difficulty with higher order motor control tasks felt to be dependent on these systems, yet have preserved general motor function.
A total of 63 children-ADHD and matched controls-completed experimental motor tasks that required maintenance of internal motor representations and the ability to inhibit visually driven responses. Children also completed a measure of motor inhibition, and a portion of the sample completed general motor function tasks.
On motor tasks that required them to maintain internal motor representations and to inhibit automatic motor responses, children with ADHD had significantly greater difficulty than controls, yet on measures of general motor dexterity, their performance was comparable. Children with ADHD displayed significantly greater intraindividual (subject) variability than controls. Intraindividual variability (IIV) contributed to variations in performance across the motor tasks, but did not account for all of the variance on all tasks.
These findings suggest that children with ADHD may be more controlled by external stimuli than by internally represented information, possibly due to dysfunction of the medial motor system. However, it is likely that children with ADHD also display general motor-execution problems (as evidenced by IIV findings), suggesting that atypicalities may extend to both medial and lateral motor systems. Findings are interpreted within the context of contemporary theories regarding motor dysfunction in ADHD, and implications for understanding externalizing behaviors in ADHD are discussed.
Attention deficit hyperactivity disorder; executive functions; motor control; motor dysfunction; motor systems
Attention Deficit Hyperactivity Disorder (ADHD) is one of the most commonly diagnosed psychiatric disorders in childhood, present in approximately 5% of school-age children. The Combined and Hyperactive-Impulsive presentations of ADHD (the ADHD subtypes of focus in this research) are defined by externalizing behaviours including hyperactivity, impulsivity, restlessness, and behavioural dysregulation. However, despite the fact that the clinical symptoms of ADHD are essentially ‘motor problems’, motor function in this population has been largely understudied and there is disagreement regarding the specific motor deficits that characterize ADHD. Of the aspects of motor function that have been studied, problems with inhibiting motor responses (resisting an action or stopping an action already in motion), selecting appropriate motor responses, flexibly adjusting one’s motor behaviour, and preparing for action have been documented in ADHD. Other evidence of motor dysfunction has been found through increased Intra Individual Variability (IIV) in ADHD. IIV defined as moment to moment fluctuations in response time on repetitive tasks and is considered to be a general marker of motor execution problems.
Research into the neural systems that are dysfunctional in ADHD indicates atypically low levels of brain activation in frontal (medial) brain systems. These frontal-medial motor systems are thought to be responsible for higher order aspects of motor function including guiding motor behaviour based on goals and mental representations, flexibly modifying behaviour in response to environmental cues, and resisting or suppressing habitual (automatic) behaviours that are not appropriate for a given context. ADHD research has also suggested atypically high levels of brain activation in basic parietal (lateral) motor systems responsible for executing well-established motor programs and for automatic responding to environmental stimuli. This research suggests an imbalance in systems responsible for controlling automatic and goal-directed motor behaviour in ADHD, which may be at the root of the externalizing behaviours seen in this population.
Figure 1. Illustration of medial and lateral motor system
Our earlier research explored this potential motor systems imbalance in ADHD through investigating a phenomenon called Utilization Behaviour (UB). UB is a clinical phenomenon seen in patients who have damage to specific frontal (medial) brain systems in the context of intact lateral-parietal systems. Behavior under these circumstances is disproportionately influenced by visual stimuli that automatically activate motor programs, which may be appropriate given an object but inappropriate for the context (e.g., reaching out and drinking from your doctor’s coffee cup on the desk in his office), interfering with goal-directed motor behaviour. This type of behaviour has been frequently described in ADHD. Indeed our prior research showed that children with ADHD do demonstrate UB and that UB is significantly associated with levels of hyperactivity, but not inattention (Archibald, Mateer, Kerns, 2001).
As a further extension of this research we investigated this motor systems imbalance through performance on specific motor tasks. We hypothesized that children with ADHD would show deficits on higher order motor tasks presumed to rely on frontal-medial motor systems, yet not show deficits on tasks of basic motor function presumed to rely on the lateral-parietal system. We also hypothesized that children with ADHD would show evidence of unusual levels of IIV in their reaction times and that IIV would be related to their performance on motor tasks.
Sixty-three children, either with ADHD or matched controls, completed a variety of motor tasks. To assess general motor function, children completed the Grooved Pegboard and Finger Tapping tasks. The Grooved Pegboard Task assesses basic motor dexterity through having children place small pegs into a grooved board as quickly as possible with both their dominant and non-dominant hands. The Finger Tapping Task assesses basic motor speed, by requiring children to tap with their index finger of their dominant and non-dominant hands as fast as possible. Children with ADHD did not differ from controls on these basic motor tasks.
To assess higher order (frontal) motor function, children completed a variety of motor tasks that required them to maintain internal motor representations (i.e., mental image of what one intends to do) and to inhibit automatic responding when presented with visually distracting information.
First, children completed a Computerized Motor Inhibition Task consisting of compatible (i.e., responding in an automatic fashion) and incompatible (i.e., resisting automatic responding in favor of a novel response) conditions (Casey et al., 1998). On the compatible condition of this task, children pressed a button on the left side of a response bar when they saw a left pointing arrow on the left side of the computer screen, a button on the right side of a response bar when they saw a right pointing arrow on the right side of the computer screen, and a middle button on a response bar when they saw an arrow in the centre of the computer screen pointing up. For the incompatible condition, their responding was reversed such that they pressed the right button to the left sided arrow and the left button to the right sided arrow. This task consisted of 240 trials and it was the task from which IIV estimates for response times were calculated. As expected, on the incompatible portion of this task children with ADHD demonstrated significantly greater difficulty with motor inhibition than controls, when they were required to suppress an automatic response in favor of a novel response. Children with ADHD also showed significantly higher levels of IIV across the task than controls.
Figure 2: Motor Inhibition Task errors by group
Second, children completed two different computerized drawing tasks. Each of these tasks manipulated visual feedback or obscured vision in some way while children were drawing, in addition to including control conditions that assessed basic drawing ability. On the Stirling Drawing Task (Stirling, Hellewell, & Ndlovu, 2001; Stirling, Hellewell, & Ouraishi, 1998), children drew designs with a computer stylus with their hand obscured. Under one condition they were able to see the designs while drawing and under the other (invisible) condition they could not see what they were drawing (i.e., computer screen was blank). The computer then generated 6 designs (one of which was the actual design they had drawn) and children were required to select their own design from among the 6 choices. The ‘invisible’ portion of this task required children to maintain a mental image of their own drawing, in order to select the correct choice. On the Computer Drawing Task (Mlakar, Jensterle, & Frith 1994), children drew shapes on a computer screen using a joystick and keyboard with their hand obscured. There were three conditions including one where they could see what they were drawing, one where the computer screen was blank, and one where the visual feedback was incompatible with their drawing (e.g., randomly drawn lines appeared on the computer screen, timed to their drawing motions). In order to draw the shapes under the ‘invisible’ and ‘incompatible’ conditions, children had to maintain a mental image of what they were drawing and ignore either the blank screen or distracting visual feedback. As hypothesized, on the Stirling Drawing Task, children with ADHD had disproportionately greater difficulty than controls on conditions where they received no visual feedback. On the Computer Drawing Task children with ADHD were significantly more impaired than controls by the incompatible visual feedback.
Figure 3: Stirling Drawing Task errors by group
Figure 4: Computer Drawing Task errors by group
Finally, children completed a Mirror Drawing Task, where they traced with a paper and pencil two simple figures in a mirror drawing device. The mirror drawing device was set up such that children could see neither their hand nor the paper and the only feedback that they received was reversed visual feedback from within the mirror. In order to perform this task correctly, children needed to ignore the reversed visual feedback presented by the mirror and to maintain an internal mental image of the correct direction in which to move their hand. On the Mirror Drawing Task, children with ADHD had much greater difficulty than controls. They made significantly more errors overall and were slower to learn the task (as seen through a more shallow learning curve or smaller reduction in errors over time when compared with controls).
Figure 5: Mirror Drawing Task errors by group
Our results partially supported, but did not fully support, our hypotheses. As suspected, and consistent with the research literature, children with ADHD did not have greater difficulty than controls on basic motor tasks assessing hand dexterity and finger tapping speed. In addition, when compared to controls, children with ADHD showed significantly higher levels of IIV and disproportionately greater difficulty on higher order motor tasks that required them to maintain internal motor representations (particularly in the face of distracting visual feedback) and inhibit automatic responding. However, interestingly, once IIV was controlled for (i.e., basic instability in motor execution (IIV) was statistically removed from our motor findings) the significant effects from all but our two most challenging tasks (Mirror Drawing and Computer Drawing) disappeared. It appeared that while IIV didn’t account for all of the variance in motor tasks, it was a significant contributor to the motor findings in this study.
Our results suggest that while children with ADHD may be more controlled by external stimuli and less so by internal (goal-directed) mental representations, they also have problems with basic motor instability. One explanation for our findings is the possibility that children with ADHD have problems with both frontal/medial (higher order) and parietal/lateral (basic) motor systems. It may be that children with ADHD compensate for basic motor system instability by recruiting frontal motor systems, systems which typically only come on-line when one is performing higher-order (complex, goal-directed) motor tasks. In recruiting limited-resource frontal systems to accomplish basic/automatic tasks, fewer resources might be available to engage in more complex motor tasks and other frontally-based tasks (i.e., tasks of working memory, executive function, etc.). While these findings support notions that ADHD is a motor disorder and that motor dysfunction is a part of the clinical picture of this disorder, it is clear that more research is required to elucidate specific motor deficits in this population, the neural systems implicated, and to make crucial links between motor dysfunction and actual behavioural symptomatology in ADHD.
Archibald, S. J., Kerns, K. A., Mateer, C. A., & Ismay, L. (2005). Evidence of utilization behavior in children with ADHD. Journal of the International Neuropsychological Society, 11(4), 367–375.
Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A., & Rapoport, J. L. (1998). Implications of right frontostriatal circuitry in response inhibition in attention deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 36(3), 374–383.
Mlakar, J., Jensterle, J., & Frith, C. D. (1994). Central monitoring deficiency and schizophrenic symptoms. Psychological Medicine, 24, 557–564.
Stirling, J. D., Hellewell, J. S. E., & Ndlovu, D. (2001). Self-monitoring dysfunction and the positive symptoms of schizophrenia. Psychopathology, 34, 198–202.