Senior Seminar - Beyond the Two-Factor Model of the ASD Diagnostic Criteria

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REVIEW

CURRENTOPINION Autism spectrum disorder in infancy: developmental considerations in treatment targets

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a b c

Jessica A. Brian , Susan E. Bryson , and Lonnie Zwaigenbaum

Purpose of review

This review explores recent literature to prioritize aspects of development to be targeted by intervention for infants and toddlers with autism spectrum disorder (ASD).

Recent findings

Recent investigation of early development in ASD, including prospective studies of infants at increased risk (i.e., those with an affected older sibling) identifies impairments in four key developmental domains that are predictive of ASD. These domains are early attentional control, emotion regulation, social orienting/ approach, and communication development. Reciprocal relationships exist among these domains, both in ASD and in typical development. Thus, these domains represent key intervention targets, informing treatment models under investigation in recent clinical trials.

Summary

By targeting the earliest and foundational manifestations of atypical development, we can capitalize on neural plasticity and build skills that are most likely to have scaffolding effects on development. The optimal timing and procedures of intervention remain empirical questions, but as the field moves toward earlier identification of risk, we are now poised to evaluate the impact of tailored approaches before the developmental cascade that leads to ASD is fully manifested. Consideration regarding community translation of ASD-specific interventions for infants and toddlers is also needed, with a focus on feasibility, cost-effectiveness, and sustainability.

Keywords

attention, autism, communication, early intervention, emotion regulation

aBloorview Research Institute, University of Toronto, Ontario, bDepartments of Pediatrics and Psychology, Dalhousie University, Halifax and cDepartment of Pediatrics, University of Alberta, Edmonton, Canada

Correspondence to Dr Jessica A. Brian, Bloorview Research Institute, 150 Kilgour Rd, Toronto, Ontaio M4G 1R8, Canada. Tel: +1 416 425 6220 x3716; fax: +1 416 422 7045; e-mail: [email protected]

Curr Opin Neurol 2015, 28:117–123

DOI:10.1097/WCO.0000000000000182

INTRODUCTION

Remarkable progress has been made in early detec- tion and diagnosis of autism spectrum disorder (ASD), particularly in high-risk samples (e.g., younger siblings of children with ASD; see [1

] for a recent review). This, in turn, has highlighted the need for developmentally appropriate interven- tion for infants and toddlers with suspected or diag- nosed ASD. Information on the nature and efficacy of such interventions is beginning to emerge [2–4]. However, to date there has been little discussion of what should constitute the main targets of inter- vention, and why. Knowing that resources are limited and time is precious, it is critical to focus on targets that yield the greatest benefits. Such endeavors are limited by current knowledge about early development of ASD, and therefore should be considered ‘moving targets’ to be refined as knowl- edge accumulates. Nonetheless, we argue that a focus on empirically and theoretically relevant targets (and associated outcomes) is warranted. This approach differs from that traditionally adopted in

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intervention for preschoolers with ASD, wherein the focus has been on the model or techniques adopted (i.e., applied behavior analysis, naturalistic and/or developmental), and on the intensity of interven- tion. Although our choice of key targets depends heavily on normative development, our operating assumption is that all of these approaches have merits, and thus an integrated model of interven- tion is warranted.

We begin by identifying early signs of ASD that might serve as intervention targets. Then, upon considering the relative precedence and putative benefits of each to overall development, we argue

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KEY POINTS

� Prospective, longitudinal studies of high-risk infants indicate early impairments in four broad domains of development that are predictive of ASD: sensory-motor, attentional, social-emotional, and communication.

� We argue for reciprocal relationships among early attentional control, emotion regulation, social orienting/approach, and early communication development in the emergence of ASD.

� With the goal of optimizing development as efficiently as possible, we propose that very early intervention should target attentional control, positive effect, social orienting/engagement, and communication.

� By targeting the earliest and foundational manifestations of atypical development, we can capitalize on neural plasticity and build skills that are most likely to have scaffolding effects on development.

� As the field moves toward earlier identification of risk, we are now poised to evaluate the impact of tailored interventions before the developmental cascade that leads to ASD is fully manifested.

Developmental disorders

for the importance of some over others (i.e., ‘key targets’). This analysis considers potential ramifica- tions of very early intervention for both psychologi- cal and neurological development in ASD. Finally, we conclude by discussing approaches and tech- niques that might be most effective in enhancing key target skills. With an eye to community trans- lation of ASD-specific interventions, we end by discussing practical issues related to feasibility, cost-effectiveness, and sustainability.

EARLY SIGNS OF AUTISM SPETRUM DISORDER AND ASSOCIATED INTERVENTION TARGETS Prospective, longitudinal studies of high-risk infants indicate that early impairments in four broad domains of development – sensory-motor, atten- tion, social-emotional, and communication – are predictive of later ASD diagnoses. Atypical develop- ment in each of these domains has the potential to disrupt early interactions with the social and non- social world, with cascading effects as development unfolds. As the field moves toward ever earlier detection of ASD risk, we are afforded the opportu- nity for earlier intervention, possibly before the full- blown syndrome has emerged and associated dys- functional neural pathways become engrained.

Sensory-motor development Although relatively little is known about sensory- motor development in infants with ASD, early

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differences have been reported based on retrospec- tive video review in the first year of life [5,6]. Pro- spective findings from high-risk infants include reduced motor activity [7], delayed motor mile- stones or atypical developmental trajectories [8–10], unusual mannerisms/repetitive behaviors, and various sensory sensitivities or interests [11 –14]. Atypical visual exploration of toys (and spinning and rotating) has been demonstrated as young as 12 months in infants later diagnosed with ASD [15]. In a study of grasping behavior, the com- ponent process, starting at 12 months, that distin- guished high-risk infants later diagnosed with ASD, was difficulty in disengaging visual attention from the object to be grasped [16]. Subtle motor delays and sensory issues have been reported as early as 6 months in babies later diagnosed with ASD (e.g., reduced motor control [11,15], protracted head lag [17]).

To date, the sensory-motor domain has not been addressed specifically in infant and toddler interven- tions for ASD, although its potential importance is underscored by theoretical links between sensory- motor and cognitive development [18,19]. Based on recent findings [16], interventions aimed at improving coordination of movement with atten- tion (e.g., reaching/grasping with coordinated eye gaze to an object) may be beneficial, although the impact of such strategies in infancy has yet to be systematically evaluated.

Attention

Deficits in attentional control, and related influences on emotion regulation, may play a central role in the emergence of ASD. The ability to disengage attention, which typically develops by 4–6 months, allows infants to move attention away from arousing events, and thereby to regulate their state [20]. Attention is largely reflexive (or involuntary) early in life, but toward the end of the first year, voluntary, or exec- utive, control over visual attention emerges, at which point emotion regulation also improves [21,22]. A selective deficit in attentional disengagement is well documented in ASD [23,24

,25] and has been demonstrated by age 12 months in high-risk infants later diagnosed with ASD [26

,27]. The relative absence of attentional control might explain the intense, prolonged negative emotional states and reduced social approach reported in infants later diagnosed with ASD [28] (S.E. Bryson, N. Garon, T. McMullen, et al., unpublished observation). Dimin- ished attentional control and difficulty regulating emotional state may together negatively impact social approach and reduce infants’ opportunities to experience positive associations from interactions

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with caregivers. Impaired attentional disengagement may also impact the development of other important functions, including joint attention and early recep- tive language (S.E. Bryson, N. Garon, T. McMullen, et al., unpublished observation). Schietecatte et al. [29] have demonstrated a relationship between atten- tional disengagement and initiating joint attention in 3-year olds with ASD; disengagement from an object of interest is arguably necessary to move atten- tion to a person. As well, early language acquisition requires flexible attention to objects or events to which others are referring when using linguistic terms. We thus argue for reciprocal relationships among early attentional control, emotion regulation, social orienting/approach, and early communication development in the emergence of ASD (cf, [30]).

Deficits in attentional control have yet to be targeted systematically in any known infant/toddler interventions for ASD, although recent work with symptomatic high-risk infants as young as 9 months has begun to encompass attention and engagement [2]. Fostering attentional control will likely be best addressed via both structured and naturalistic inter- vention methods. Wass et al. [31] have successfully used a series of computerized gaze-contingent orienting tasks with typically developing 11-month olds, with evidence of enhanced cognitive control, sustained attention, and attentional disengage- ment. Attention-training programs such as this clearly hold promise for use with high-risk infants. However, given documented challenges generaliz- ing from contrived to real-world situations in ASD [32], the inclusion of training in a naturalistic con- text may be a critical addition. Gains in attentional control could lead to downstream effects on emotion regulation, social engagement, and joint attention, which in turn might further foster com- munication development.

Social-emotional development Early social-emotional deficits in ASD include reduced positive affect and reciprocal social smiling, reduced social orienting, and atypical face process- ing.

Positive facial affect (i.e., smiling) is thought to have innate hedonic value that serves to motivate the development of very early social-communi- cation skills such as eye gaze and reciprocal social smiling [33 –35]. These very early interactions are also essential to the development of the emotional connectedness (or inter-subjectivity) required for understanding others, which is impaired in ASD [36 –38]. The putative significance of shared positive emotion to subsequent communicative and social development, together with converging evidence of its early impairment in ASD, argues for targeted

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interventions. Reduced facial expressiveness, particularly smiling, is well documented in pre- schoolers with ASD [39,40], and reduced smiling has been reported by 12–18 months in infants sub- sequently diagnosed with ASD [7,10,12,41], but not earlier (e.g., [42]). The possibility remains that diminished social smiling is a consequence of earlier deficits in orienting to others.

Early home videos of infants later diagnosed with ASD initially revealed reduced social orienting toward the end of the first year of life [5,43]. Evi- dence of even earlier deficits in attention to faces comes from high-risk samples, although discrepan- cies exist as to the timing of its emergence, the specific facial regions involved, and even specificity to ASD. Some studies fail to find group differences until 12 or 18 months [10,44], whereas others have reported differences as early as 6 months [45]. Chawarska et al. [45] reported reduced attention to a video-displayed static face in 6-month-old infants later diagnosed with ASD; however, diminished attention to the video screen also distinguished this group, suggesting that attentional control may be the more primary issue. Selective deficits in orienting to faces have not been replicated consist- ently in experimental paradigms. For example, Elsabbagh et al. [46] did not report a difference in looking time toward eyes of static faces between low-risk controls and high-risk infants (including those later diagnosed with ASD) at 6–10 months, although there were differences in evoked responses related to ASD outcome. In a related study, high-risk infants (aged 6�10 and 12�15 months) were shown displays containing faces and nonsocial stimuli. This task also failed to distinguish infants who went on to have ASD [44]. Instead, a nonspecific effect emerged, whereby high-risk infants (regardless of ASD out- come) spent marginally more time looking at faces and less time sampling other items in the visual display. Based on infants’ eye gaze while watching videos of actors looking directly into the camera and making age-appropriate social overtures, Jones and Klin [47] reported a declining trajectory of eye-looking time in high-risk infants later diagnosed with ASD relative to high-risk and low-risk controls beginning at 2 months of age, although cross- sectional differences were not detectable until 9 months of age. This body of work highlights the importance of controlling carefully for stimulus characteristics such as face region assessed and the nature of the display (dynamic vs. static). It also remains possible that other features can account for differences in looking time. For example, one possibility is that motion is the critical variable in observed differences between response to eyes and mouths in dynamic displays.

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Thus, despite early evidence of reduced social orienting in ASD, findings remain somewhat incon- sistent when examined experimentally in very young babies. Further research is needed to more fully understand the nature, timing, and specificity of this phenomenon. Moreover, competing views remain as to the primacy of a basic attentional vs. social interpretation of atypical social orienting in ASD. Elsabbagh et al. [44] interpret their findings as evidence of deficient attentional control, conclud- ing that ‘cortical mechanisms mediating efficient selection and distribution of attention appear to modulate infants’ early responses to faces’ (p. 153). Nonetheless, both basic attention and social orienting deficits appear to index early- developing challenges in brain and behavioral func- tioning, which may, at a minimum, interact in a cascading manner to contribute to ASD outcomes. As such, both can be argued to be critical targets for intervention in infants and young toddlers with emerging ASD.

Interventions aimed at fostering early social- emotional development in ASD may need to focus first on increasing child orienting to a social partner and parent responsiveness [4,48]. Some existing parent- or teacher-mediated approaches with tod- dlers have yielded gains related to social orienting or engagement [49 –51]. Through increased social orienting, opportunities arise to foster positive affect sharing through approaches that capitalize on the child’s motivation and interests, and on building positive, reciprocal interactions with social partners. Moreover, given the relationship between positive affect and both learning in general [52], and social engagement specifically [35,53], learning may be enhanced by targeting positive affect directly. Whether this is accomplished best by directly targeting child and/or caregiver smiling (e.g., via parent-mediated interventions) remains an empiri- cal question, but evidence suggests that this is best accomplished through the use of naturalistic behav- ioral procedures that capitalize on the child’s motiv- ation, such as those of Pivotal Response Training [2,54].

Communication

Early communication differences in ASD include reduced nonverbal and verbal communication such as lack of eye gaze and pointing to share interest (i.e., joint attention), diminished use of gestures, reduced babbling and reduplication, delayed receptive word learning, and few if any words used mean- ingfully [1

,55 &

]. Most communication deficits are not clearly apparent until the end of the first year and usually manifest as the absence of typical

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development (vs. deviance, which tends to emerge later; e.g., idiosyncratic or repetitive language in the second year).

Impairments in joint attention are well docu- mented in ASD [29,56,57]. Because joint attention typically develops within the first year, this has been an area of considerable interest in early ASD detec- tion research [58 –61]. However, despite the widely held view that joint attention deficits are universal in ASD, variances in task demands can yield differ- ent effects. An intriguing phenomenon highlighted by Jones et al. in their review [1

] is that orienting to a proximal target may be relatively less impaired in ASD than orienting to a more distal target. They posit that joint attention to near objects may occur via reflexive orienting mechanisms, whereas distal orienting may require greater motivation and understanding of the referential nature of the orienting cue. Selective deficits in distal orienting are consistent with an attentional interpretation whereby executive, or voluntary, control of atten- tion is needed for distal, but not more proximal (i.e., reflexive), orienting.

Some of the earliest communication impair- ments in ASD may emerge in response to deficits in attentional control and its impact on skills like joint attention. However, regardless of whether communication deficits are primary or at least par- tially secondary to more basic deficits in attention, communication development (including within the context of overall intelligence [62]) has taken pre- cedence as a target in ASD-specific interventions for toddlers, for several reasons. First, communication deficits remain among the most easily detected first signs in clinical contexts, leading to the bulk of referrals for assessment. Moreover, communication may be viewed as a key target because it lays the foundation for meaningful interactions with care- givers and others, prevents or reduces behavioral agitation, and remains the best predictor of positive outcomes in ASD [63].

As the next generation of infant intervention programs are developed, the challenge will be to design strategies that address the earliest manifes- tations of communicative deficits in ASD. These will ideally include methods for fostering nonverbal communicative acts such as eye-to-eye gaze, gesture use, and functional vocal output, prior to the devel- opment of verbal language. Such skills will be most appropriately taught in naturalistic contexts, capitalizing on highly motivating interactions and social routines (thereby optimizing positive effective states), with tight, but developmentally appropriate contingencies between the babies’ communicative acts and responses from communi- cation partners (e.g., primary caregiver, therapist).

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Evidence is beginning to emerge regarding the effi- cacy of such strategies used with infants in the first year of life [2], revealing that such interventions have the potential to positively affect outcomes in a meaningful way.

SUMMARY OF KEY INTERVENTION TARGETS

Although several systems have been implicated, findings on early development in ASD most consist- ently point to poor attentional control, reduced positive emotion, and delayed nonverbal and verbal communication skills, atypical development in any of which has the potential to disrupt early inter- actions with the world, contributing to cascading effects as development unfolds. Findings on social orienting and attention to faces are less consistent, especially with respect to timing, but important, given the nature of the social challenges in ASD. With the goal of optimizing development as effi- ciently as possible, we thus suggest that very early intervention should target attentional control, social orienting/engagement, positive affect, and communication. By targeting the earliest and foundational manifestations of atypical develop- ment, we can capitalize on neural plasticity [64,65] and build skills that are most likely to have scaffolding effects on development. Evidence dis- cussed above also implicates complex interactions between the earliest-developing deficits in ASD, highlighting the potential for wide-reaching, collateral effects of intervening in key domains. The optimal timing and procedures of intervention in these domains remain empirical questions, but as the field moves toward earlier identification of risk, we are now poised to evaluate the impact of tailored interventions before the developmental cascade that leads to ASD has the opportunity to take hold.

PRACTICAL CONSIDERATIONS

Given current prevalence [66], future intervention efforts must focus on community translation of ASD-specific interventions, with a focus on feasible, cost-effective, and sustainable programs. Current evidence supports the efficacy of resource-intensive (i.e., 1 : 1), comprehensive, behaviorally based approaches for use with preschoolers [67]. As we move to earlier, publicly funded models, creative approaches are needed to maintain efficacy with more children in need and fewer resources. Parent-mediated approaches that capitalize on the principles of applied behavior analysis as well as those of naturalistic learning are gaining traction

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with infants and toddlers [3], often with a focus on child-directed and highly motivating activities. These are appealing because they are a natural fit for this age group, and because they afford the opportunity for intensive intervention by teaching parents skills that can be integrated into everyday caregiving interactions. By identifying key targets that are likely to have collateral effects on multiple domains and by capitalizing on evidence-based intervention methods, we will be poised to deliver efficient and effective intervention very early in development in a sustainable way.

CONCLUSION

Evidence from high-risk longitudinal cohorts indicates that atypical development may first appear in the sensory-motor system, with deficits in atten- tional control by the latter part of the first year. Such deficits are associated with concomitant impair- ments in emotion regulation, possibly affecting social approach and joint attention, and negatively impacting the development of positive associations required to fuel the social reward system [68]. Moreover, basic deficits in attentional control may result in reduced social orienting, also nega- tively affecting infants’ opportunities to learn from and about social partners. Deficits in attentional control may also impact important foundational social communicative interactions such as joint attention and affect sharing. Mounting evidence points to a cascading effect of these differences over the first year of life and into the second year. By carefully considering the nature by which these differences unfold, we have the opportunity to develop very early interventions targeted to key processes that have the potential to have a scaffold- ing influence on development. Intervention at the earliest possible time points, if appropriately targeted, has the potential for significant down- stream effects including secondary prevention of suboptimal outcomes.

Acknowledgements

None.

Financial support and sponsorship

Our research is supported by the Canadian Institutes of Health Research, Autism Speaks Canada, the Simons Foundation, the Sinneave Family Foundation and NeuroDevNet. L.Z. is supported by the Stollery Child- ren’s Hospital Foundation Chair in Autism.

Conflicts of interest

There are no conflicts of interest.

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