Elsevier

Neuroscience & Biobehavioral Reviews

Volume 47, November 2014, Pages 559-577
Neuroscience & Biobehavioral Reviews

Review
Impairments to visual disengagement in autism spectrum disorder: A review of experimental studies from infancy to adulthood

https://doi.org/10.1016/j.neubiorev.2014.10.011Get rights and content

Highlights

  • Disengage deficit appears in first year of life in infants who have ASD.

  • Dynamic stimuli are more likely to cause a disengage deficit in ASD.

  • At longer ISI durations, people with ASD are not different from controls.

Abstract

Impairments in visual disengagement are a current focus of research in autism spectrum disorders (ASD) and may play a key role in the early expression of social–emotional deficits associated with the disorder. This review summarizes current knowledge of visual disengagement and orienting in ASD. Convergent reports from infancy to adulthood indicate that (1) impairments to visual disengagement are apparent on Gap–Overlap tasks, spatial orienting tasks, and tasks involving social stimuli; and (2) these impairments emerge in the first year of life and continue into adulthood. The relationships between visual disengagement, orienting, joint attention, emotional regulation, and IQ are discussed in relation to ASD.

Introduction

Attention is broadly defined as information processes that mediate perceptual selection (Colombo and Cheatham, 2006). Attentional selection is controlled by two integrated processes: an endogenous, top-down goal-directed process that is dependent on desires, expectations, and/or knowledge of the individual, and an exogenous, bottom-up stimulus-driven process that may be at odds with goal-directed behaviours (Yantis, 1993, Wolfe, 1994). Posner and Petersen (1990) and Petersen and Posner (2012) have argued that attention consists of three functionally independent attention networks: the alerting, orienting, and executive control networks. The alerting network allows the individual to maintain a state of alertness; the orienting network directs attention to specific sensory stimuli and locations; and the executive control network allows the resolution of conflicting attentional information. Because attention is the mechanism through which we view our world, thereby determining what we experience and respond to, an early-developing disorder that interferes with attention may have far reaching effects on cognitive development (Fischer et al., 2013).

Autism Spectrum Disorders (ASD) are developmental disorders characterized by impairments in social-communication and the presence of repetitive or restricted behaviors (American Psychiatric Association, 2013). ASD is one of the most prevalent forms of developmental disability internationally, with current estimates at 1 in 68 (Centers for Disease Control and Prevention, 2014). Impairments to attention have often been considered to be associated or comorbid with the disorder (Keehn et al., 2013), although recent research has suggested that attentional abnormalities play more of a primary role in ASD, underlying several core features, including the impairments in emotional regulation (Bryson et al., 2004, Gardner et al., 1992, Anderson and Colombo, 2009, Garon et al., 2009), and in joint attention (Schietecatte et al., 2012, Morales et al., 2000, Mundy et al., 2007), as well as the inflexibility in behaviour (Hutt et al., 1964, Landry and Bryson, 2004, Lovaas et al., 1979, Casey et al., 1993, 2001; Senju et al., 2004). Not surprisingly, impairments to the alerting network, the orienting network, and the executive control networks have been reported in ASD (for an overview of atypical attention in ASD using the three network model, see Keehn et al., 2013).

Impaired visual orienting is the earliest attentional deficit reported in infants at-risk for ASD (high-risk by virtue of having an older sibling diagnosed with ASD) (Elsabbagh et al., 2009, Zwaigenbaum et al., 2005). The purpose of this review is to provide an in-depth examination of research that has examined the disengagement operation of visual orienting in individuals with ASD. This research will be examined using a developmental framework, which assumes that atypical attention processes may have implications for the emergence and ongoing evolution of the ASD phenotype (Keehn et al., 2013). This developmental framework makes the initial assumption that abnormal disengagement of attention represents a primary disturbance in ASD and may serve as an early marker for identifying infants at-risk for ASD.

For the purpose of identifying the existing literature on visual disengagement in ASD, systematic searches were performed in four computerized bibliographic databases: PUBMED, ISI WEB of Science, PsycINFO, and BIOSIS. LRS performed the search using the following terms: ‘autism’ and ‘diseng*’ OR “orienting.” The search results were independently replicated by VLA. Additional articles of interest were located by hand searching the reference sections of the identified articles. Fig. 1 illustrates our search strategy, methods adopted from The PRISMA Group (Moher et al., 2009). To be included in the review, a paper had to: (1) examine visual disengagement in individuals with ASD or at-risk of a later diagnosis of ASD, (2) include a comparison group of typically developing children (TD; without a family history of ASD), and possibly other comparison groups, such as children with other forms of developmental delay, and (3) confirm ASD diagnoses using standardized diagnostic instruments. Thirty-seven articles met inclusion criteria and were included in the body of the review.

Key findings from these articles are presented below, beginning with an overview of the development of visual orienting in typically developing (TD) children, followed by examinations of visual disengagement in infants, adolescents, and adults with ASD using various methodologies. The review ends with a discussion of the implications of impairments to orienting visual attention and how these may relate to the risk of ASD.

Section snippets

Typical development of the visual orienting network

Visual attention refers to the ability to direct and sustain visual focus on an action or event (Vivani et al., 2008). Visual orienting towards and away from stimuli is the primary means of exploring the world during infancy and is comprised of three successive components of spatial attention (Posner and Cohen, 1984). First, disengagement of attention is the breaking of visual attention from a fixated stimulus; second, shifting attention is the movement of visual attention from a previously

Visual disengagement during the Gap–Overlap task

The Gap–Overlap task is a computer-based task that measures the latency to begin an eye movement (also termed saccadic reaction time) from a central stimulus after the appearance of a peripheral stimulus. The task includes two or three trial types, depending on the study. In the Overlap trial, the central stimulus remains on screen and overlaps in time with the peripheral stimulus. In a Gap trial, the disappearance of the central stimulus and the appearance of the peripheral stimulus are

Visual disengagement during spatial orienting

The spatial orienting task is a computerized spatial attention task similar to that developed by Posner and Cohen (1984). In the standard version of the task, the central fixation point is a white cross, which is flanked by green, square boxes on the left and right of the central fixation point. Each trial begins with the brightening of one of the two flanking boxes following a short or long ISI. An asterisk appears in either the brightened (cued) box for valid trials or the non-cued box during

Visual disengagement during spatial cueing in ASD with cerebellar damage

Research characterizing deficits in individuals with acquired brain injury (ABI) have noted that impairments in visual disengagement involve activity in the parietal cortex (Posner et al., 1987, Pierrot-Deseilligny et al., 1995). Imaging reports of individuals with ASD, however, have noted that the most consistently reported site of neuroanatomical abnormalities in the ASD brain is the cerebellum (Townsend et al., 1996a, Courchesne et al., 1994). To understand the role of cerebellar damage in

Visual disengagement during tasks with social stimuli

The following section will describe research examining the role of social stimuli during visual disengagement in children with ASD. As cumulative modelling of ASD symptomology makes differential predictions in terms of brain systems sub-serving social versus non-social cognition (Elsabbagh and Johnson, 2010), there is the potential for differences in visual disengagement from social versus non-social cues between individuals with ASD and their TD peers. Impairments in disengaging from social

Discussion

There is robust evidence from early development, childhood, and adulthood that visual disengagement is impaired in ASD. Prospective examination of visual disengagement during the first years of life suggest that impairments to visual disengagement are apparent by 12 months of age in HR infants who later receive a diagnosis of ASD (Bryson et al., 2014, Elsabbagh et al., 2013, Sacrey et al., 2013, Zwaigenbaum et al., 2005). Furthermore, these impairments continue into childhood and adulthood, as

Conclusion

Abnormal visual disengagement is an early marker of ASD, with most studies reporting that it emerges in the latter half of the first year of life (Zwaigenbaum et al., 2005, Elsabbagh et al., 2013, Elison et al., 2013, Sacrey et al., 2013). Visual disengagement is an important component of visual orienting, allowing a child to disengage from a current locus of interest and shift attention to a secondary locus (Posner, 1988). This ability is an important component of social–emotional regulation,

Acknowledgements

This research is supported by CIHR and Autism Speaks Canada. LRS is supported by a CIHR Autism Research Training Program Postdoctoral Fellowship award. VLA is supported by a research fellowship from the IWK Health Centre. SEB is supported by the Craig Chair in Autism Research and the Dalhousie Medical Research Foundation. LZ is supported by the Stollery Children's Hospital Foundation Chair in Autism Research and an Alberta Innovates-Health Solutions Scholar Award.

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