Looking at social characteristics of autism through sensory relativism

Talking about autism, people usually think about difficulties in social communication and restricted and repetitive patterns of behaviours, interests or activities. What is less commonly known is that people in the autism spectrum often experience sensory sensitivity symptoms, to the point that the new edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-5) has incorporated ‘hyper- or hypo-reactivity to sensory input or unusual interests in sensory aspects of the environment’ as possible symptoms. These sensory characteristics begin to emerge in infancy and can be noticed when parents say things like "My child startles easily at sound" or "My child is distressed having nails trimmed". This does not mean that every child startling easily at sounds is going to be autistic. Like any trait, sensory sensitivity is distributed as a continuum across the general population, and researchers don’t consider sensory alterations among possible causes for autism. However, it becomes more and more evident with time and studies that sensory and socio-communicative symptoms are closely related (Mandy et al., 2012) and this relationship must be considered carefully in individual treatments (Karmiloff-Smith, 1998).

Sensory symptoms can be divided into three main constructs: hypersensitivity, hyposensitivity, and sensation seeking (Boyd et al., 2010). Hypersensitive children have low neurological threshold to external stimuli, meaning that they keep processing even the tiniest stimuli. These children experience difficulty maintaining attention to a single task among competing stimuli, and thus tend to show distractibility and hyperactivity. Hyposensitive children, on the contrary, have high neurological threshold to external stimuli, meaning that stronger stimuli are needed to elicit a response in those children. They often appear dull or uninterested, and often show low tone and sedentary behaviors. Finally, children described as sensation seeking actively strive to meet their high neurological threshold by engaging in behaviors to increase their sensory experiences. These children show high impulsivity, high excitability and lack of caution. Since sensory sensitivity symptoms are present from the earliest stages of development in autism, before clear socio-communicative symptoms emerge, it is possible that they could affect early social development by altering the child's sensory experience of a wide range of stimuli, including social stimuli (Baranek et al., 2006). Supporting this hypothesis, parent concerns about sensory behaviour at 6 months of age are strongly associated to later diagnosis of autism (Sacrey et al., 2015), and 12-month-old infants later diagnosed with autism show more frequent and intense distress reactions to a variety of sensory stimuli (Zwaigenbaum et al., 2005). Researchers tend to agree on the association between hyposensitivity and more severe social and communication symptoms (Watson et al., 2011). However, hypersensitivity may sometimes be associated with better social communicative functioning, particularly in early development (Green et al., 2011).

Behavioural observations of such association between alterations in sensory processing and social behaviour and/or communication are problematic in terms of interpretation because of the multiple neurocognitive processes that underlie performance. Electrophysiology is an infant-friendly technique that allows researchers to examine the association between more specific neurocognitive processes and symptoms observed.  Specifically, event-related potentials (ERPs) measure neural responses to specific events (like a visual stimulus) with great detail in time, and can be successfully collected from awake infants and toddlers. Recently, researchers have started to use ERPs to investigate the relationship between sensory sensitivities and attention capture by visual stimuli (Webb et al., 2013; Jones et al., 2018), and how this affects the emergence of symptoms in social behaviour and communication that are characteristic of autism. Attention capture is a candidate mechanism through which sensory sensitivities may act to alter a child’s learning experience of the social and non-social environment (Green et al., 2016). In a naturalistic environment, people possess many low-level features that typically engage attention, such as motion, audiovisual synchrony and unpredictability. You might expect then individuals with higher levels of hypersensitivity to capture attention more easily and more strongly than others do (Baranek et al., 2006). Since attention capture shapes learning (Dayan et al., 2000; Roelfsema et al., 2010), social development might even be facilitated by heightened sensory sensitivities, as observed within some groups of children with autism (Watson et al., 2011; Green et al., 2011). Thus, researchers examine early ERP responses in infancy to investigate individual differences in attention capture.

People are typically more salient in the child's environment because they move, talk and are unpredictable. The child thus tends to pay more attention to them. In this dynamic scenario, the development of social skills likely depends on how much attention children pay to people around them, and how much they learn from them. Now, imagine what can happen if infants experience sensory alterations and just don’t perceive things like we do. Imagine if they are more sensitive and go visit family, they will probably have lot of people staring at them, hugging and kissing and touching, then of course they will get overwhelmed and probably try to avoid them or even have a tantrum. Or if they are less sensitive and happen to be in a dangerous situation where mom looks worried to them as a warning, but they will not get that and go on, they will likely get hurt. And what if children who do not do well in school simply can't cope well with the sensory environment they experience in class? What if we can find a way to adapt the environment to the child's needs and optimise the learning experience, thus likely improving long term outcome? To do this, we need to understand the possible mechanisms underlying sensory processing, attention and resulting social behaviours. But how can we investigate these sort of mechanisms? We need something simple to perform experiments on from an early age but also key to elicit this sort of response in the infant and able to capture these complex dynamics underlying social attention, learning and sensory processing. The answer is faces. 

Infants are bombarded with faces right from birth. Just think about them being continuously exposed to mom’s face, or daddy’s, or those of all family and friends coming to visit. Everybody looks at the infant right in the face and smiles, laughs, shows any possible kind of emotion. Infants learn much more than you can imagine from that. They learn about emotions, language, shared interests, engagement with others, in brief, the fundamentals of social skills and communication. That’s why researchers like me focus so much on how infants process faces and how this relates to their social skills later in life. We see a broad range of differences in the way infants as young as 6 months of age who later develop autism process faces, gaze and visual noise stimuli in terms of brain response to those stimuli. Individual differences in this response are associated to different sensory sensitivity and social skills at 3 years of age. Specifically, enhanced response to faces predicts better social skills in toddlerhood already from the first year of life in the individual infant (Tye, Bussu et al., 2020). This is likely due to the development of expertise in processing faces, and social stimuli in general, which leads to better learning from the social environment surrounding the child, eventually leading to higher social skills. This process is strongly dependent on the sensory characteristics of individual infants, in terms of how they perceive stimuli from the environment, but also in terms of how they react to that and adapt to it. We still have much work to do to understand how sensory processing and attention to social stimuli like faces relate to each other over development, and how this links to social functioning later in life. However, we know it is critical to take it account a child’s sensory profile to optimize the environment in crucial settings like schools or more specifically therapeutic environments for children with autism.

Baranek, G.T., David, F.J., Poe, M.D., Stone, W.L., Watson, L.R., 2006. Sensory Experiences Questionnaire: discriminating sensory features in young children with autism, developmental delays, and typical development. J. Child Psychol. Psychiatry 

Boyd, B.A., et al., 2010. Sensory features and repetitive behaviors in children with autism and developmental delays. Autism Res. Off. J. Int. Soc. Autism Res.

Dayan, P., Kakade, S., Montague, P.R., 2000. Learning and selective attention. Nat. Neurosci.

de Haan, M., Johnson, M.H., Halit, H., 2003. Development of face-sensitive event-related potentials during infancy: a review. Int. J. Psychophysiol. Off. J. Int. Organ. Psychophysiol. 

Green, S.A., Ben-Sasson, A., Soto, T.W., Carter, A.S., 2011. Anxiety and sensory overresponsivity in toddlers with autism spectrum disorders: bidirectional effects across time. J. Autism Dev. Disord.

Green, S.A., Hernandez, L., Bookheimer, S.Y., Dapretto, M., 2016. Salience network connectivity in autism is related to brain and behavioral markers of sensory overresponsivity. J. Am. Acad. Child Adolesc. Psychiatry

Jones, E.J.H., Dawsons, G., Webb, S. 2018. Sensory hypersensitivity predicts enhanced attention capture by faces in the early development of ASD. Developmental Cognitive Neuroscience

Karmiloff-Smith, A. 1998. Development itself is the key to understanding developmental disorders. Trends in Cognitive Sciences

Mandy, W., Charman, T., Skuse, D.H. 2012. Testing the Construct Validity of Proposed Criteria for DSM-5 Autism Spectrum Disorder. Journal of the American Academy of Child & Adolescent Psychiatry

Roelfsema, P.R., van Ooyen, A., Watanabe, T., 2010. Perceptual learning rules based on reinforcers and attention. Trends Cogn. Sci. 

Sacrey, L.-A.R., et al., 2015. Can parents’ concerns predict autism spectrum disorder? A prospective study of high-risk siblings from 6 to 36 months of age. J. Am. Acad. Child Adolesc. Psychiatry 

Tye, C.*, Bussu, G.*, Gliga, T., Elsabbagh, M., Pasco, G., Johnsen, K., Charman, T., Jones, E.J.H.#, Buitelaar, J.K.#, Johnson, M.H.#, and the BASIS team. 2020. Understanding the nature of face processing in early autism: A prospective study. MedRxiv doi: 10.1101/2020.05.06.20092619 *shared first authorship #shared last authorship

Watson, L.R., et al., 2011. Differential associations between sensory response patterns and language, social, and communication measures in children with autism or other developmental disabilities. J. Speech Lang. Hear. Res. 

Webb, S.J., et al., 2013. Guidelines and best practices for electrophysiological data collection, analysis and reporting in autism. J. Autism Dev. Disord. http://dx.doi.org/ 10.1007/s10803-013-1916-6. 

Zwaigenbaum, L., et al., 2005. Behavioral manifestations of autism in the first year of life. Int. J. Dev. Neurosci. 23, 143–152.