Review article
Autism spectrum disorder and attention-deficit/hyperactivity disorder in early childhood: A review of unique and shared characteristics and developmental antecedents

https://doi.org/10.1016/j.neubiorev.2016.03.019Get rights and content

Highlights

  • Connects research on early symptoms, temperament and cognition in ASD and ADHD.

  • Attention problems may be a common pathway to ASD and ADHD.

  • Proposes a motivational model for temperament differences between ASD and ADHD.

  • Low effortful control may have different underpinnings in ASD and ADHD.

  • Discusses the role of executive function in the pathways to ASD and ADHD.

Abstract

Autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD) have overlapping characteristics and etiological factors, but to which extent this applies to infant- and preschool age is less well understood. Comparing the pathways to ASD and ADHD from the earliest possible stages is crucial for understanding how phenotypic overlap emerges and develops. Ultimately, these insights may guide preventative and therapeutic interventions. Here, we review the literature on the core symptoms, temperament and executive function in ASD and ADHD from infancy through preschool age, and draw several conclusions: (1) the co-occurrence of ASD and ADHD increases with age, severity of symptoms and lower IQ, (2) attention problems form a linking pin between early ASD and ADHD, but the behavioral, cognitive and sensory correlates of these attention problems partly diverge between the two conditions, (3) ASD and ADHD share high levels of negative affect, although the underlying motivational and behavioral tendencies seem to differ, and (4) ASD and ADHD share difficulties with control and shifting, but partly opposite behaviors seem to be involved.

Introduction

ASD and ADHD are neurodevelopmental disorders that share an early onset, delays and deviances in the development of brain structure/function, cognitive impairments, a male preponderance, and strong genetic influences on individual differences and liability (Rutter et al., 2006). Over the past decade, research has indicated that symptoms of ASD and ADHD frequently co-occur in the same individuals and cluster within families (de Bruin et al., 2007, Melegari et al., 2015, Simonoff et al., 2008, Hofvander et al., 2009, Lundstrom et al., 2011). Further, both conditions have overlapping characteristics and etiological factors (see Posthuma and Polderman, 2013, Rommelse et al., 2010, Rommelse et al., 2011, Ronald et al., 2010b, Taurines et al., 2012 for reviews). However, most of this research has been conducted in middle childhood and early adolescence. To which extent ASD and ADHD overlap or differ at the level of overt characteristics, brain mechanisms and etiology at infant and preschool age is less well understood.

There are important reasons for studying the development of ASD and ADHD and their phenotypic overlap from the earliest possible stages. Both ASD and ADHD, like most psychopathological conditions, develop from interactions among multiple genetic and environmental influences on a network of neurobiological systems that begin to unfold in prenatal life (Rutter, 2011, Sonuga-Barke and Halperin, 2010). These interactions explain why distinct impairments and risks in ASD and ADHD show varied developmental trajectories and outcomes (see Elsabbagh et al., 2011, Sonuga-Barke, 2005, Thapar et al., 2013, Willcutt et al., 2012 for reviews). Studying the associations between ASD and ADHD in the first years of life makes it possible to examine whether and how phenotypic overlap emerges and develops, and whether the development of one disorder or dysfunction leads to the development of the other(s); or alternatively, whether distinct disorders or dysfunctions originate from a common set of early risk factors. Further, study at very young age may allow the identification of the behavioral, cognitive, neural, genetic and environmental processes that precede/underlie the expression of clinical symptoms of ASD and ADHD. Ultimately, insight in these early processes may have implications for preventative and therapeutic interventions (Sonuga-Barke and Halperin, 2010, Yirmiya and Charman, 2010).

Here, we review the literature on the early signs and developmental antecedents of ASD and ADHD. We focus on the core behaviors, temperament and cognition in children up to preschool age and highlight the unique and shared characteristics of both conditions. Doing so, we partly build on a recent review focusing on early markers for ASD and ADHD in infants at risk (M.H. Johnson et al., 2014). Up till now, research in ASD has an obvious lead over ADHD as regards the precursors and early signs and has recently been discussed in four reviews (Elsabbagh and Johnson, 2010, Jones et al., 2014, Yirmiya and Charman, 2010, Zwaigenbaum et al., 2013). There is only one review explicitly comparing the early characteristics of ASD and ADHD (M.H. Johnson et al., 2014); Our review adds to this review (1) by including not only studies with children at familial risk but also studies with clinical and population samples, allowing to examine the characteristics in a wider range of severity of ASD and/or ADHD, (2) by an in depth focus on the core symptoms, temperament and early emerging executive function in ASD vs ADHD. This is relevant as co-morbidity may be a result of interactions among such characteristics over time, conform a network approach to disorders and co-morbidity (Borsboom and Cramer, 2013, Borsboom et al., 2011) instead of being merely a result of latent constructs, (3) by extending the age range to preschool years (up to 7) in contrast to previous reviews. This is of particular relevance since many characteristics, in particular neurocognitive capacities, while emerging in the first months of life, continue to undergo important changes during the 3rd to 6th year. We chose for a qualitative review approach because of the inclusion of a wide range of data on ASD and ADHD from a disparate literature that does not lend itself to a quantitative pooling of results, in line with the directives for reviews highlighted by (Nigg, 2012).

Several issues that explain the approach and focus of the present review warrant consideration. First, ASD and ADHD are both heterogeneous conditions. Symptoms of ASD and ADHD range from mild and even subclinical traits in the general population to fully developed clinical disorders (Coghill and Sonuga-Barke, 2012, Constantino, 2011, Frazier et al., 2007, Lubke et al., 2009). As similar heritability estimates have been found across different levels of severity in ASD and in ADHD (Larsson et al., 2012, Robinson et al., 2011), similar etiologic factors may operate along the continuum of severity. Therefore, we include both studies reporting on subclinical, quantitative traits as well as clinical symptoms of ASD and ADHD. Second, both ASD and ADHD encompass distinct core symptom domains with (partly) differing heritability and course. In ASD these domains are the social-communicative vs restrictive-repetitive behavior domains (Happe and Ronald, 2008, Robinson et al., 2012), and in ADHD the hyperactivity-impulsivity vs inattention domains (Frazier et al., 2007, Greven et al., 2011a, Greven et al., 2011b, Nikolas and Burt, 2010). Third, valid assessment of early signs in the core domains of ASD and ADHD is compromised by the uneven maturational course of different skills and corresponding impairments (Pauli-Pott and Becker, 2011, Pauli-Pott and Becker, 2015). Specifically, several core symptoms of ASD generally manifest at an earlier age than the core symptoms in ADHD. ASD may reliably be diagnosed from about the second year (Yirmiya and Charman, 2010, Zwaigenbaum et al., 2013), whereas the first signs of ADHD show much overlap with ubiquitous ADHD-like behaviors and only become predictive of ADHD from about preschool age onwards (Leblanc et al., 2008, Sonuga-Barke and Halperin, 2010, Wahlstedt et al., 2008). This is why early emerging dysfunctions like those in attentional processes, and temperamental traits are of particular interest in very young children as these may represent more direct risk markers of atypical development than later emerging clinical phenotypes (Elsabbagh et al., 2011, Elsabbagh and Johnson, 2010, Gurevitz et al., 2014, Nigg et al., 2004). Alternatively, early emerging dysfunctions may act as modifiers of the phenotype and developmental course of ASD and ADHD (Clifford et al., 2013, Johnson, 2012, Mundy et al., 2007). Hence, in this review we take into consideration behavioral measures belonging to the core domains as well as measures of temperamental and cognitive domains.

Section snippets

Identification of studies

We searched with PubMed and Web of Science for peer reviewed English-language research articles published between 2000 and February 2015. The following search terms were used: autism (spectrum) (disorder), ASD, attention deficit (hyperactivity) (disorder), and ADHD in combinations with: co-morbidity, attention (deficit), hyperactivity, impulsivity, social (communication), repetitive behavior, cognition, neuropsychology, executive function, temperament, effortful control, at (high-)risk, early

Core behavioral characteristics

The co-occurrence of ASD and ADHD symptoms or traits in early childhood has been investigated using two different approaches, by examining either the pairwise associations between DSM-defined full diagnoses of ASD and ADHD, or the presence of symptoms or traits of ASD and/or ADHD in clinical or population based samples (see Appendix Table A1, for a summary of included studies).

Temperament

Temperament traits can be defined as constitutionally based individual differences in the domains of activity, affectivity, attention, and self-regulation that are the product of interactions among genetic, biological, and environmental factors across time (Shiner et al., 2012) and that can be linked to neurobiological systems (Karalunas et al., 2014, Posner et al., 2012, Rothbart et al., 2011). The traits emerge early during development, are relatively stable and show a normal distribution in

Executive function

Cognition is a general term for the mental processes involved in gaining meaning and knowledge from information and selecting appropriate responses in order to adapt flexibly to the ever changing environments. Both higher-order and more basic functions are involved in cognition with largely known neuronal underpinnings that are etiologically linked to- and may alter- development, such as information processing and executive function (EF) (Johnson, 2012, Keehn et al., 2013, Russo et al., 2007,

Discussion

With the present review of the literature on the core symptoms, temperament and cognition in relation to ASD and ADHD during infancy and preschool age, we identified unique and shared characteristics in the early trajectories of ASD and ADHD. In the following sections we discuss several theoretical implications and the challenges raised by the literature.

Challenges and recommendations for future research

In the next section we elaborate on limitations of the current literature for allowing conclusions about early unique and shared antecedents of ASD and ADHD, and provide recommendations for future research.

Clinical implications

This review provides a basis for several clinical implications regarding assessment, early recognition and treatment recommendations for co-occurring ASD and ADHD. In view of the strong clinical overlap, children referred for ASD should also be assessed for ADHD (traits) and vice versa, which also implies that clinicians should look for ASD problems in the context of ADHD and for ADHD- and emotion regulation problems in ASD.

Given the complex and prolonged developmental trajectories in many

Conclusions

Several preliminary conclusions can be drawn from this review on the shared or unique early behavioral and cognitive characteristics of ASD and ADHD: 1) core symptoms or traits of ASD and ADHD frequently co-occur, and this co-occurrence increases with age, severity of symptoms and lower IQ; 2) attentional problems form a linking pin between ASD and ADHD but the behavioral, cognitive and sensory correlates partly diverge between the two conditions; 3) ASD and ADHD share high levels of negative

Conflict of interests

Dr. Buitelaar has been a consultant to/member of advisory board of/and/or speaker for Janssen Cilag BV, Eli Lilly, Shire, Medice, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties.

Acknowledgements

Dr. Buitelaar’s work for the current paper is supported by the European Community’s Seventh Framework Program (FP7/2007-2013) under grant agreement n° 278948 (TACTICS) and n° 602450 (IMAGEMEND), and the Innovative Medicines Initiative Joint Undertaking under grant agreement number 115300 (EU-AIMS), resources of which are composed of financial contribution from the European Union's Seventh Framework Program (FP7/2007-2013) and the European Federation of Pharmaceutical Industries and Associations

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