Signs of atypical visual behaviour have been detected by the naked eye much earlier than the emergence of ASD traits (Jones et al., 2014). For example, Feldman et al. (2012) found that parents noticed reduced interest in faces and attention shifts from a toy to the person during play interactions in their 12-month-old children who later received a diagnosis of ASD. Similarly, less gazes to faces were reported at 12 months of age and less eye-contact at 18 months of age during experimenter-delivered standardized assessment (Ozonoff et al., 2010). These reports have encouraged researchers to deeply investigate subtle differences in looking behaviours in infants at high familial risk for ASD. The most robust findings are summarised below.
3.1.1.1 “Sticky fixation” style
As mentioned in Chapter 1, Zwaigenbaum and colleagues (2005) provided evidence for atypical looking behaviour underlying attention orienting from multiple sources of observation in 12- month-old infants with emerging ASD. Measures from parent-reports, researcher-administered behavioural assessment and the ‘gap-overlap’ task, a marker task for the ability of disengaging the gaze from a central stimulus to direct attention to a peripheral stimulus, converged in identifying a tendency to fixate on particular objects at the expense of a more active exploration in infants who later received a diagnosis of ASD. This ‘sticky fixation’ style has been shown to be
predictive of higher ASD severity measured with the ADOS (Lord et al., 2000) at 24 months (Zwaigenbaum et al., 2005).
In typical development, “sticky fixation” is the definition for a behaviour observed in 1-month- old babies who have difficulties in shifting their gaze away from a target of fixation. This behaviour emerges as a sign of the first, non-modulated cortical influences on oculomotor control (Johnson & De Haan, 2015). Following dendritic growth and myelination between the cortical visual cortex and other cortical areas, developmental changes occur in attention skills regulating disengagement in typical infants, mainly in the first 6 months of age (Colombo & Cheatham, 2006). Blaga and Colombo (2006) reported that after this age disengagement latencies measured with a gap-overlap task are not particularly affected by manipulations of the stimulus designed to affect visual processing. They argued that, in typical development, individual variability in look duration and cognitive concomitants is less influenced by differences in disengagement from the second half of the first year (Blaga & Colombo, 2006). In atypical development, however, difficulties in disengagement might consolidate during the first year and re-emerge in the second year. For example, Elsabbagh et al. (2013) found that a “sticky fixation” attention style, characterised by difficulties in disengaging from the central stimulus in a gap-overlap task, was observed in HR infants with later ASD at 13 months, although not at 7 months. Similarly, Sacrey, Bryson, & Zwaigenbaum (2013) found that prolonged latency to disengage from a manipulated object during play was only observed from 12 months of age in HR infants who later received a diagnosis of ASD, and remained at 15, 18 and 24 months. Thus, the “sticky fixation” style emerges at the end of the first year of life in infants who will later develop core ASD symptoms. These disengagement difficulties have been shown to play a role in the developmental trajectory of ASD (Bedford et al., 2014). One possibility is that difficulties in the ability to disengage from distracting objects and look at a person’s face or referent in joint attention situations might reduce possibilities for learning in social contexts. Bedford et al. (2016) found that latencies in disengagement were associated with later social communication difficulties in 13-month-old boys at risk for ASD. Differently, Keehn, Müller, & Townsend (2013) suggested that early impairments in disengagement, reflecting early inefficiencies in the orienting network in infants with emerging ASD, may have implications for the development of efficient executive control processes. This assumption was based on a study by Posner, Rothbart, Sheese, & Voelker (2012), who found that orienting to novel sensory information during infancy predicted effortful control at 3 and 4 years. Effortful control is a major form of self-regulation and consists in the ability to inhibit a dominant response to perform a subdominant response and to engage in action planning. Because monitoring and resolving conflicts between incompatible responses require voluntary and attentive control, this
construct is considered a function of executive attention (Rothbart & Rueda, 2009). Based on their results and on the literature on brain networks, neuromodulators and genetic contributions to attention orienting and executive attention, Posner and colleagues (2012) postulated that early orienting to novel stimuli may activate executive network functions necessary for self-regulation (Posner et al., 2012).
Thus, difficulties in disengagement have been consistently found to be early markers of ASD in at risk infants after the first year of life. To what degree the “sticky fixation” style is an early manifestation of the narrow-attention style characteristic of ASD or impact the development of social, communication and executive function acquisition has not been clarified yet.
3.1.1.2 Staring at faces
Atypicalities in looking behaviour in 1-year-old or older infants at familial risk for ASD have been also detected using eye-tracking during a face pop-out paradigm. This task consists in presentations of arrays of different objects including a face. It was originally designed to assess exogenous orienting towards a face stimulus such that if a typical orienting mechanism biased towards faces is in place, the infant is expected to direct her gaze to the face first. Elsabbagh, Gliga, et al. (2012) examined this performance in HR infants and found that infants who later received a diagnosis of ASD showed intact face orienting. Surprisingly, however, by 14 months of age these infants showed overall longer looking time at the face stimulus compared with typically developing infants.
Hendry et al. (2018) replicated this finding in an independent cohort, using a different measure which has been demonstrated to have high intra-individual consistency across tasks (Wass, 2014): the duration of the longest look (peak look) at the face. They found that HR infants who later received a diagnosis of ASD showed longer peak look durations at the face stimulus than LR controls. However, HR infants who did not receive an ASD diagnosis at age 3 also showed longer peak look durations at the face compared to LR infants. Of note, atypically long duration of the peak look was observed when infants were attending to faces specifically, while no group difference was found in peak look duration to non-social stimuli (Hendry et al., 2018). Interestingly, the rate of change in peak look duration from the first to the second year was predictive of effortful control but not of social difficulties at 3 years of age (Hendry et al., 2018). Further, studies examining peak look durations to faces versus objects in habituation tasks found longer peak looks to faces in 12-month-old infants with emerging ASD (Jones et al., 2016; Jones, Dawson, Kelly, Estes, & Webb, 2017). In 18- to 30-month-old toddlers with ASD, longer peak
look durations during habituation to faces were associated with poorer social skills and lower verbal abilities, suggesting that indeed this looking behaviour might be tightly linked to ASD symptoms (Webb et al., 2010). In addition, evidence supporting a causal link between this early sign and later ASD traits comes from an intervention study showing that peak look duration at the face during habituation was reduced at 18 months following parent-delivered intervention aimed to improve social skills (Jones et al., 2017). Of note, this intervention had also the effect of normalising neural correlates of attention engagement (amplitude of the P400 ERP component) in response to faces at 12 months of age, suggesting that shallower neural processing during social attention might lead to slower learning and hence be reflected in slower habituation (Jones et al., 2017).
In sum, there is converging evidence that looking time at a static face stimulus might be involved in the path to ASD, although there are mixed findings with respect to which of the features of ASD might be more closely related to this early sign of atypicality: autistic social traits, communication difficulties or disrupted executive functioning.
3.1.1.3 Responding to joint attention
As reviewed in the Chapter 1 (see section 1.2.3), social attention, considered as the allocation of attentional resources to conspecifics (Salley & Colombo, 2016), contributes to the development and partly correspond to the ability to direct our own attention in the direction of attention of other people (Mundy, 2018). This milestone of social cognition is called “responding to joint attention” (Mundy & Newell, 2009), and it has been studied widely in the ASD literature using “gaze following” paradigms (Salley & Colombo, 2016). The first signs of atypical processing of gaze direction in ASD have been observed between 6 and 10 months as failure to show neural signatures of gaze shift processing around 400 ms after the stimulus onset (P400 amplitude) unlike what observed in typically developing infants (Elsabbagh, Mercure, et al., 2012).
Additionally, using eye-tracking systems it has been possible to also study looking behaviour of infants when watching another person shifting the gaze towards an object. By 10 months, infants at high risk for ASD show reduced ability to direct their attention to the referent object (i.e. the gazed-at object) when only eyes shifts, without a concurrent head turn, are performed in naturalistic interactions (Thorup, Nyström, Gredebäck, Bölte, & Falck-Ytter, 2016). Similarly, Bedford et al. (2012) found that by 13 months infants at high familial risk for ASD show decreased attention engagement to the object to which the other person’s gaze moved. This sign, which has been interpreted as difficulty in understanding the communicative relevance of
eye-gaze, was predictive of later social communication impairment in HR children (Bedford et al., 2012).
Importantly, attention engagement to the gazed-at object and disengagement difficulties have been shown to contribute to ASD in an additive manner, suggesting that they might reflect different manifestations of early diversions from the typical developmental trajectory (Bedford et al., 2014). As anticipated in the introduction, in neurodevelopmental disorders the development of the complex network underpinning attention, which includes circuits devoted to perceptual and memory processes, might be disrupted due to an inefficient combination of feedforward and feedback influences between visual areas and more-rostral cortical areas, including parts of the parietal, frontal and temporal cortices involved in visual attention (Amso & Scerif, 2015). In the case of the development of joint attention, atypical connectivity in neural networks affecting feedforward input from lower to higher cortical regions might lead to failure to direct attention to gaze shifts and in turn prevent the developing brain from obtaining important feedback information about the referent object (Amso & Scerif, 2015), with cascading effects on spontaneous learning in social context (Csibra & Gergely, 2011). Thus, it is possible that early neural disruption of the attention system in infants at risk for ASD lead to inefficient responding to joint attention at later stages, but this hypothesis has not been supported by data yet, to my knowledge. Importantly, the ability of infants to be sensitive to referential cues has been argued to be an important aspect of the human communication system what enables social learning (Csibra & Gergely, 2009). Thus, this looking behaviour in infancy is expected to have an impact on later social and communication skills.
In sum, this section summarises evidence showing that atypical looking behaviour emerges after the first year of life in HR infants who later develop core ASD symptoms. In particular, difficulties in disengagement precede later ASD (Bedford et al., 2014; Elsabbagh et al., 2013; Zwaigenbaum et al., 2005); longer looking time at static face stimuli has been shown to be predictive of social difficulties (Elsabbagh, Gliga, et al., 2012; Jones et al., 2016) as well as language impairment (Webb et al., 2010) and low executive function (Hendry et al., 2018)in childhood; reduced engagement with the object towards which a person directs her gaze or the person’s face predicts later autism-like social difficulties and social adaptive behaviour (Bedford et al., 2012; Chawarska, Macart, & Shic, 2013). In the following section I review two frameworks for interpreting a possible role of atypical looking behaviour in the path to ASD.