Mechanisms of deficit of visuospatial attention shift in children with developmental coordination disorder: A neurophysiological measure of the endogenous Posner paradigm

Abstract

The purpose of this study was to investigate and compare the mechanisms of brain activity, as revealed by a combination of the visuospatial attention shifting paradigm and event-related potentials (ERP) in children with developmental coordination disorder (DCD) and typically developing children. Twenty-eight DCD children and 26 typically developing children were recorded with regard to their behavioral performance and ERP measures during a variant of the endogenous Posner paradigm, in which they should react to visual targets preceded by spatial cues or presented uncued. Children with DCD showed longer reaction time and a deficit in inhibitory response capacity when compared to typically developing children. The electrophysiological characteristics also showed distinct modulatory effects upon attentional orienting, anticipatory mechanisms, and cognitive-to-motor transfer in children with DCD: longer cue-P3 and target-N1 latency, smaller target-P3 amplitude, an elongated interval between N2 and the motor response (N2-RT), and small areas on contingent negative variation (CNV). The combined analysis of behavioral performance and ERP data suggested that children with DCD had deficits of slower target identification (N1), less ability in interhemispheric (P3) and cognitive-to-motor transfer speed (N2-RT), as well as a less mature anticipatory and executive process (CNV).

Introduction

Developmental Coordination Disorder (DCD), in the Diagnostic and Statistical Manual of Mental Health Disorder (DSM-IV) of the American Psychiatric Association and the ICD-10 Classification of Mental and Behavioral Disorder in Children and Adolescents from the World Health Organization, is a term related to poor motor proficiency that is not the result of specific neurological diseases or other psychiatric, physical, or medical problems (American Psychiatric Association, 1994, WHO, 1992, WHO, 1996). In spite of the absence of any other disorder, DCD interferes significantly with the child’s academic achievement and normal daily activities (Henderson & Hall, 1982). More importantly, DCD has been demonstrated to often persist into adolescence and early adulthood, along with associated psycho-social problems (Cantell et al., 1994, Visser et al., 1998).

Although the explicitly etiological significance of DCD is still unclear, the definite deficits demonstrated are motor control impairments (Cherng et al., 2007, Tsai et al., 2008), neural constraints (Sigmundsson et al., 1997a, Sigmundsson et al., 1997b, Sigmundsson et al., 1999), and more neurological soft signs (Lundy-Ekman, Ivry, Keele, & Woollacott, 1991) in children with DCD as compared to typically developing children. Some researchers from the neurobehavioral models of inter- and intra-sensory functioning have formulated hypotheses that the mechanism of DCD seems to be related to right hemisphere insufficiency or dysfunctional corpus callosum (Sigmundsson et al., 1997a, Sigmundsson et al., 1997b, Sigmundsson et al., 1999). Neuropsychological and psychological studies have also made an effort to find out whether DCD is specifically impaired in motor function or in isolated cognitive processing, or is involved in both cognitive and motor disorders. Although the results are still inconclusive, numerous studies have suggested that children with DCD display deficits in perceptual or perceptual-motor functioning (Bonifacci, 2004, Lord and Hulme, 1987, Lord and Hulme, 1988, Sigmundsson et al., 2003, Tsai et al., 2008, Tsai and Wu, 2008, Van Waelvelde et al., 2004, Wilson and McKenzie, 1998). Furthermore, it has been suggested that the mechanism of impairments of motor coordination is most pronounced on and strongly associated with low-level perceptual function, especially with a deficiency related to visuospatial information processing (Tsai and Wu, 2008, Tsai et al., 2008, Wilson and McKenzie, 1998).

Since the neuroanatomical bases of dysfunction in children with DCD are indistinct, speculations on the potential neuropathology can utilize theories of the cognitive anatomy of attention (Swanson et al., 1991). As a result, different versions of covert orienting of endogenous and exogenous visuospatial attention tasks (e.g., the Posner paradigm) with different stimulus onset asynchrony (SOA) (Tsai et al., 2009, Wilson and Maruff, 1999, Wilson et al., 1997), the classic Simon task (Mandich et al., 2002, Tsai et al., 2009), and some visuospatial cue tasks (Mandich et al., 2003, Wilmut et al., 2007) have been employed with the base on the neuropsychological domain in order to explore the potential mechanism of motor deficits. Although the general slowing of responses best reflects the motor impairments that occur as part of DCD, children with DCD display a selective visuospatial deficit only in shifts of volitional (endogenous) but not dislocation of automatic (exogenous) attention (Mandich et al., 2002, Mandich et al., 2003, Tsai et al., 2009, Wilson and Maruff, 1999, Wilson et al., 1997).

The Posner paradigm (Posner, 1980), owing to an important characteristic of attentional control within the region of visual space in the absence of eye movements and with minimal motor element involvement, has been considered to appropriately assess the deficit of visuospatial information processing in children with DCD (Tsai, 2009, Tsai et al., 2009, Wilson and Maruff, 1999, Wilson et al., 1997). In order to produce efficient behavior during performance of the Posner paradigm task, subjects have to apply selective attention regarding the plastic ability to prioritize processing of certain stimulus features (Correa, Lupianez, Madrid, & Tudela, 2006). In covert orienting of a visuospatial attention task in the endogenous Posner paradigm, children are asked to react to visual target stimulus after centrally delivered cues pointing to the correct target side (i.e., valid condition) or the opposite side (i.e., invalid condition) (Posner and Cohen, 1984, Wilson and Maruff, 1999, Wilson et al., 1997). In some of the trials, no directional information related to the two potential locations for the target is given, to keep attention diffused and alert in the neutral (non-cued) condition. The endogenous Posner paradigm can be interpreted at a cognitive level and procedurally motivate volitional/intentional movement, and is also more dependent on the activation of cortical attention areas, such as posterior parietal cortex and frontal lobes (Posner and Cohen, 1984, Wilson et al., 1997). This endogenous facilitation seems to result in widespread cortical activation to attain volitionally generated shifts of attentional resources (Mayer, Dorflinger, Rao, & Seidenberg, 2004). Since the attention network test involves alerting, orienting, and executive attention, which are associated with different specific brain areas, the endogenous Posner paradigm can efficiently assess individual difference in cerebral responses (Fan et al., 2002, Posner et al., 2007).

ERP recordings made during the Posner paradigm task performance permitted on-line measures of shifts of attention in the order of milliseconds, as well as the assessment of the consequences of visual and motor processing of the stimuli, which cannot be obtained by behavioral performance alone (Purves et al., 2008). A network of brain areas used in focusing visual attention to spatial locations has been discovered (Corbetta and Shulman, 2002, Nobre, 2001, Perchet and Garcia-Larrea, 2000, Perchet and Garcia-Larrea, 2005), demonstrating early electrophysiological activity over the occipital region for perceptual processing and late electrophysiological activity related to decision-making and motor processes (Mangun, 1995). Furthermore, the posterior parietal region is concerned with covert orienting and the redirecting of it (Corbetta and Shulman, 2002, Rushworth et al., 2003). Some researchers have found that children aged 6–9, when performing the exogenous Posner task, already have well developed simpler cognitive processes with the ERP reflections (Perchet and Garcia-Larrea, 2000, Perchet and Garcia-Larrea, 2005). Therefore, within a single recording session, the possibility of examining the ERP concomitants of different cognitive axes – anticipatory processing prior to actual target stimulus, attentional priming of different cued stimuli, target identification, and response selection – seems to be warranted in children.

The endogenous visuospatial attention task coupled with ERP recording have been demonstrated to evoke the different visual response components on ERP: early visual responses N1 modulation reflect stimulus triggered orienting and engagement of voluntary visuospatial attention to relevant stimulus locations (Fu et al., 2008, Griffin et al., 2002, Luck et al., 1990), and late potential activities, such as N2 for response inhibition processes (Kok, 1986) and P300 (P3) for cognitive responses (i.e., motor processes) (Griffin et al., 2002, Linden, 2005).

In sum, notwithstanding the behavior deficit of inhibitory response capacity during completion of endogenous visuospatial attention orienting tasks which has been demonstrated in children with DCD (Mandich et al., 2002, Tsai, 2009, Tsai et al., 2009, Wilson and Maruff, 1999, Wilson et al., 1997), to the best of our knowledge, the mechanisms of both early perceptual and late motor processing in brain activity underlying such behavior anomalies have not yet been explored. Meanwhile, as described above, analysis of ERP elicited by the stimuli of cue and target should reflect the dynamics of brain activity related to the orienting of attention in time. Furthermore, it is worth mentioning that the effect sizes of correlations of motor and cognitive deficits were significant only for demanding timed motor-response items, the magnitude of which was markedly higher than that for untimed items in children with DCD (Van Waelvelde et al., 2004, Wilson and McKenzie, 1998). Taken together, the purpose of this study was to simultaneously assess the ERP and behavioral performances in children with DCD when performing the endogenous Posner paradigm task with SOA 350 ms, as compared to those of age-matched control subjects. This was not only because this topic has not previously been addressed, but also because the results from synchronous assessment of the neuropsychological and cognitive electrophysiological data can provide more compelling evidence and gain deeper insight into abnormal behavior performances. In addition, the present study can offer information on how the attentional-orienting mechanism modulates stimulus processing in the endogenous Posner paradigm task in typically developing children.