Attentional and sensory contributions to postural sway in children with autism spectrum disorder

Highlights

• Static balance was tested in children with autism and controls.

• Attentional distraction by means of a cognitive dual task had little effect on COP fluctuations.

• We found a greater destabilizing effect of closing the eyes for the autism group than for controls.

Abstract

Postural control is known to depend on sensory and cognitive factors. Little is known about how children with autism spectrum disorder (ASD) regulate static balance, and to what extent vision and cognition contribute to the regulation of balance in this group. We compared a group of children with mild ASD and a group of age- and gender-matched controls on various postural tasks, standing on a Wii Balance Board. We tested a sensory disturbance (closing the eyes) and a cognitive disturbance (word memorization) on the control of quiet standing. Analysis of center-of-pressure excursions revealed moderate effects of cognitive load, but clear effects of vision. We found a greater destabilizing effect of closing the eyes (greater postural excursions in the medio-lateral direction) for the ASD group than for controls. No group differences were found on word recall and on a standardized balance test (Movement Assessment Battery for Children; M-ABC2). We suggest that the postural effects reflect tighter coupling between vision and motor adjustments in ASD than in controls, which is consistent with recent suggestions of greater reliance on vision in this group.

Introduction

Autism spectrum disorders (ASDs) are characterized by persistent deficits in social communication and social interaction, constrained, repetitive patterns of behavior, and restricted interests or activities [1], [2]. These deficits manifest themselves in early childhood and impair every day functioning. With the introduction of the DSM-5 [2] motor abnormalities seem to figure more prominently in the diagnostic criteria of autism than in its predecessor (DSM-IV [1]). Motor problems have been frequently observed in ASD [3], [4], [5], and may involve motor planning deficits, motor coordination abnormalities, fine and gross motor skill deficits, clumsiness and postural instability [6], [7], [8]. A meta-analysis [6] showed large effects for substantial motor coordination deficits in all subtypes of ASD, associated with dysfunctions in cortical and subcortical areas including the motor cortex, supplementary motor area, basal ganglia, and cerebellum. In a similar vein, it has been argued [9] that motor abnormalities represent early and persistent clinical signs, which could serve as endophenotypes for ASD. Another review [10], however, designated it premature to relate movement disturbance as a core symptom of ASD, because empirical data were deemed not robust enough.

Yet, numerous studies have found balance problems and postural abnormalities in ASD. Balance problems in children with ASD have been found using standardized instruments, in particular the Movement Assessment Battery for Children (M-ABC) [11], [12]. Poorly developed balance skills in children – regardless of pathology – may reduce the capability to develop more complicated movement skills, which, in turn, may hamper social development and the willingness to participate in sports [13]. Furthermore, a number of studies have analyzed postural sway, and have found postural abnormalities in ASD in various postural tasks, such as quiet standing and looking straight ahead [14], [15], [16], quiet standing and dual-tasking [17], quiet standing with the eyes closed [8], quiet standing on a sway-referenced platform [18], and quiet standing while performing visual search [19]. Also, postural instability appeared related to symptom severity regarding the occurrence of repetitive behaviors [8]. These latter authors suggested that postural instability is related to core ASD symptoms.

A possible factor mediating between postural control and ASD symptomatology is attention. However, remarkably few studies have looked at attentional contributions to the regulation of balance in ASD. The role of attention in motor control in adolescents with ASD was highlighted in a recent study [20], which found that motor performance in this group, as measured by a tapping task, was related to attentional (dys)function. The authors found that motor performance was correlated to one particular attentional function, namely the efficiency by which a spatial cue is used to orient attention. If motor abnormalities are – in part – related to attentional (dys)function, then an attention-demanding secondary task should lead to even greater abnormal motor patterns. We decided to test this hypothesis in a quiet-standing paradigm. It has been shown that regulation of balance is attention demanding, even in highly skilled individuals such as dancers [21]. We tested the effect of an attention demanding cognitive activity on postural fluctuations in a group of children with a mild form of ASD, using a word memorization task [21], [22]. If individuals with ASD employ excessive cognitive resources to regulate their balance, then cognitive dual-tasking should have a destabilizing effect on this group but not on controls.

In addition, we tested the contribution of visual input to the regulation of balance in this group. Previous studies [8], [23] have found decreased postural performance in ASD when the eyes are closed. Closing the eyes leads to a shift toward other sensory modalities to regulate balance, necessitating more attention-demanding control of balance. The second aim of this study was to assess whether dual-tasking and removal of visual input leads to additive or interactive effects on postural parameters.

So, our hypotheses were that (1) cognitive dual-tasking has a destabilizing effect in ASD, and (2) standing with eyes closed also has a destabilizing effect in this group, possibly mediated by an inward attentional focus.