Deficits in the endogenous control of covert visuospatial attention in children with developmental coordination disorder
Introduction
Motor impairment in children that is not explicable in terms of any medical condition or low IQ is described by the Diagnostic and Statistical Manual (DSM-IV) as Developmental Coordination Disorder (DCD) (American Psychiatric Association, 1994). It is estimated that approximately 5–6% of children meet the DSM criteria for DCD (Henderson & Hall, 1982, Sovik & Maeland, 1986). Psychological and neuropsychological studies have attempted to isolate specific processing deficits that might underlie the disorder. A wide range of perceptual and motor control deficits have been reported. These deficits include: visuospatial perception (Hulme et al., 1982a, Hulme et al., 1982b, Hulme et al., 1984, Hulme et al., 1983, Lord & Hulme, 1987, Lord & Hulme, 1988), kinaesthetic function (Bairstow & Laszlo, 1981, Bairstow & Laszlo, 1989, Laszlo & Bairstow, 1983, Laszlo & Bairstow, 1985, Laszlo et al., 1988), crossmodal perception (Newnham & McKenzie, 1993), response selection (van Dellen & Geuze, 1990), and motor programming (Smyth, 1991). A recent meta-analysis by Wilson and McKenzie (1998)has revealed that although children with DCD perform worse than control children on most behavioural measures, deficits are most pronounced for visuospatial tasks, regardless of whether or not a motor response must be organised. Findings supported the notion that deficits in processing visuospatial information are strongly associated with difficulties in motor coordination.
Deficits in visual processing have been reported at different levels of control in these children: low-level perceptual functions (Hulme et al., 1982a, Hulme et al., 1982b, Hulme et al., 1983, Hulme et al., 1984, Lord & Hulme, 1987, Lord & Hulme, 1988); short-term visual memory (Dwyer & McKenzie, 1994, Skorji & McKenzie, 1997); and visual feedback mechanisms (Geuze & Kalverboer, 1987, Lord & Hulme, 1988, van der Meulen et al., 1991). More recently, using the covert orienting of visual spatial attention task (COVAT) (Posner, 1980), we have shown that visual processing deficits also extend to selective attention (Wilson et al., 1997).
The COVAT provides a valid and reliable measure of an individual's ability to direct visuospatial attention to areas of the visual field without accompanying eye movements. Participants are required to keep their eyes on a central fixation point and respond manually to the onset of an imperative stimulus in one of two peripheral locations, either to the left or right of fixation. The peripheral locations are usually marked by an open box or circle. Before the imperative stimulus appears, a spatial cue directs the subject's attention to one of the peripheral locations. The stimulus can then appear either at the location indicated by the peripheral cue (valid trial) or at the location contralateral to the cue (invalid trial). When the time interval between cue and imperative stimulus (stimulus onset asynchrony – SOA) is less than 200–300 ms, reaction times (RTs) to validly cued stimuli are faster than those to invalidly cued stimuli (Posner, 1980, Rafal & Henik, 1994). This facilitation is thought to occur because imperative stimuli appearing in the uncued location require that attention be (i) disengaged from the cued location, (ii) moved to the location of the imperative stimulus, and (iii) engaged on this stimulus before a manual response can be made (Posner, 1988). These extra operations require additional time to complete. As SOAs increase there is more time to complete these operations, and thus the magnitude of the difference between validly and invalidly cued trials varies across SOAs (Posner, 1980, Rafal & Henik, 1994). As well as providing spatial information, the spatial cue interrupts any non-task related processing and alerts the subject that an imperative stimulus is about to appear (Posner et al., 1987). In neuropsychological studies it has been found that lesions of the posterior parietal lobe, the midbrain, and the thalamus disrupt selectively the disengage, move and engage operations, respectively (Posner & Petersen, 1990, Posner & Raichle, 1994). The alert and interrupt operations have been shown to depend upon processing in anterior cortical structures (Posner et al., 1987). The COVAT has been used to detect subtle deficits of visuospatial attention in patients with movement disorders such as Parkinson's disease (Rafal et al., 1984, Wright et al., 1990) and Huntington's disease (Tsai et al., 1995).
COVAT studies have used two types of spatial cue to direct attention to peripheral locations: peripheral and central symbolic. Peripheral cues indicate the location of the imperative stimulus by appearing at or around its location, for example, the luminance of the circle that surrounds the location is increased suddenly. Spatial cues can also be presented at the centre of the display to indicate the location of the imperative stimulus symbolically, for example, an arrow-head pointing left or right. Facilitation of RT is found for both peripheral and central symbolic cues. However, differences between the patterns of performance to the two types of cue suggest that each operates through different attentional processing networks with peripheral cues initiating an automatic or exogenous orienting mode and central symbolic cues initiating a controlled or endogenous orienting mode. For attentional shifts signalled by central symbolic cues, facilitation disappears if imperative stimuli have less than a 60% probability of appearing at the cued location, if subjects perform a concurrent memory task, or if subjects choose to suppress the orienting response (Muller & Rabbitt, 1989, Rafal & Henik, 1994). For peripheral cues, facilitation is found without the addition of any probability information. In addition, facilitation for peripheral cues diminishes as SOAs increase beyond approximately 200–300 ms. Following this, RTs to invalid trials become faster than RTs to valid trials. This inhibition of RT to stimuli appearing at the cued location has been termed inhibition of return and does not occur for central symbolic cues (Muller & Rabbitt, 1989, Rafal & Henik, 1994). These differences indicate that the dynamics of covert orienting are dependent on the type of spatial cue used to signal attentional shifts. Moreover, each mode of orienting involves separate neural systems. The endogenous mode appears to be mediated by networks that include the posterior parietal cortex and frontal lobes (Posner et al., 1984), while the exogenous mode is mediated by subcortical structures, including the superior colliculus and thalamus (Rafal & Henik, 1994Robinson & Kertzman, 1995).
Wilson et al. (1997)examined separately the exogenous and endogenous modes of orienting in children with DCD and control children. The two groups were tested on two different COVATs with SOA (150 and 350 ms) varied randomly. For a COVAT with peripheral cues and equal probability of valid and invalid trials, RTs for valid and invalid trials at the 150-ms SOA were not significantly different between groups but RTs for valid and invalid trials at the 350-ms SOA were greater in the DCD group. The absence of any interactions involving cue type indicated that the relative RT difference between valid and invalid trials was similar for the two groups at both SOAs. Thus, for peripheral cues, the DCD group had no difficulty directing covert attention at either the 150- or 350-ms SOA. However, they did not use the additional 200 ms between cue and imperative stimulus to facilitate stimulus detection. This suggests that they had difficulty using the alerting properties of peripheral spatial cues to prepare motor responses. For a COVAT with probability-based central cues, a significant interaction effect was observed between group and cue type. Results showed that RTs for valid trials were equal in the two groups but for invalid trials children with DCD showed greater RTs regardless of SOA. This was consistent with a deficit in the voluntary disengagement of covert attention (Posner et al., 1987).
The aim of the current project was to investigate further the control of covert visuospatial attention in children with DCD and determine how generalised deficits are in this domain. By using the same COVAT paradigm but with longer SOAs, we have attempted to replicate and extend the results of our earlier studies. First, we examined the extent to which DCD children can use additional processing time between peripheral cue and imperative stimulus to facilitate the latter's detection, and whether they display the normal pattern of inhibition of return with SOAs above 350 ms. Second, by allowing more time between central cue and imperative stimulus to prepare motor responses, we examined whether these children overcome apparent deficits in the disengage operation of controlled covert orienting.
Section snippets
Participants
The sample consisted of 20 children aged 9–12 years who met the clinical criteria for DCD and 20 control children. There were 10 boys and 10 girls in each group. Selection of the DCD sample was carried out using a previously validated method (Dwyer & McKenzie, 1994). In the first stage, teachers were asked to refer children whose motor coordination was below average for their age (Criterion A for DCD, DSM-IV) and whose motor problems interfered significantly with functional motor tasks such as
ANOVA results
One control child failed to complete this task. The means of participants' median RTs for the experimental conditions are presented in the first section of Table 1 and Fig. 1. There were significant main effects for group (F(1,37)=17.48, p < 0.001) and SOA (F(1,37)=94.57, p < 0.001): RTs for controls (M=411 ms) were significantly faster than those for DCD children (M=512 ms), and RTs at the 850-ms SOA (M=430 ms) were faster than those at the 150-ms SOA (M=497 ms). The main effect for cue type was
General discussion
Results from this study support the hypothesis that DCD is associated with a deficit in the endogenous disengagement of attention while the exogenous orienting mode is not implicated in the disorder. A degree of heterogeneity within the DCD group is acknowledged, however–orienting deficits were not evident in all children. The results of each COVAT are discussed in turn. First, both DCD and control groups displayed the normal time course of covert orienting to peripheral cues; for both groups,
Conclusions
The performance of the DCD group was slower than that of the control group for both COVATs in the current study. This general slowing of responses best reflects the motor deficits that occur as part of DCD (Geuze & Kalverboer, 1987, Henderson, 1993; Schellekens et al., 1983). It is unlikely, however, that motor disabilities led to the pattern of responding found on the COVATs. The attentional deficit found in the DCD group occurred only for central probability-based cues, and motor screening
Acknowledgements
This research was supported by Grant 8992 from the Australian Research Council (Small Grants Scheme), and Starter Research Grant from the Albury-Wodonga campus of La Trobe University. For their cooperation during the collection of data we thank the staff and students of Ivanhoe Grammar (Melbourne), Brighton Grammar (Melbourne), Creek Street Christian College (Bendigo), Girton Grammar (Bendigo) and St. Mary's Primary School (Myrtleford).
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2014, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Studies that assessed both the endogenous and exogenous mode of attention consistently found that only the endogenous mode of control was impaired in DCD. Exclusion of children with ADHD (Tsai et al., 2009a,b, 2010, 2012; Tsai, 2009; Wilson et al., 1997; Wilson and Maruff, 1999) suggested that these deficits are specific to DCD and do not arise as a consequence of attentional symptoms of ADHD. Results of the included studies on covert oculomotor control should be interpreted with a degree of caution because most studies did not control for confounds and did not indicate whether all DSM-IV-TR criteria for DCD were fulfilled.