Journal of Child Psychology and Psychiatry 55:6 (2014), pp 578–581

doi:10.1111/jcpp.12254

Commentary: Becoming social – a commentary on  & Frith (2014) Happe 1

Charles A. Nelson III1,2

Department of Pediatrics, Harvard Medical School, Boston Children’s Hospital; 2Center on the Developing Child, Harvard University, Boston, MA, USA

The field of developmental cognitive neuroscience is now established as a discipline at the nexus of the broader fields of developmental psychology and cognitive neuroscience. Sitting in its rear view mirror, but gaining rapidly, is the nascent discipline of developmental social neuroscience. Given the relative youth of this field, it is not surprising that a great deal of energy has gone into generating a rich corpus of empirical data. As a result, however, we have a plethora of findings but lack a conceptual framework in which to place, integrate, and interpret them. The splendid Annual Research Review article published in this issue by Happ e and Frith (2014) addresses this shortcoming. The authors offer a scholarly account of developmental social neuroscience. Impressively, their review goes far beyond what is known about typical social development; the article also discusses a variety of disorders of development, ranging from the rare (e.g., Mobius syndrome) to the highly prevalent (e.g., autism). By including a discussion of disruptions in development, the authors achieve two goals: to educate the reader about a range of developmental disorders and to leverage what is known about these disorders to shed light on the mechanisms supporting typical social development. The Happ e and Frith article is organized chronologically, beginning with what is known about social behavior and its neural bases in the newborn, progressing through the rest of infancy and childhood, and ending in adolescence. Within each age bracket, the authors lay out the fundamental building blocks of typical development (e.g., social perception, joint attention, theory of mind) and then turn their attention to disorders of development that impact these critical social processes. For example, the social deficits that characterize autism are discussed in the context of developmental milestones during the first few years of life, whereas disrupted social cognition in social anxiety and schizophrenia spectrum disorders are referenced in the context of adolescent social development. It is the rare article that stimulates the reader’s own thinking about the subject at hand, leading one to consider topics either not tackled by the authors or touched upon lightly. Thus, in this commentary, I would like to focus my remarks on how Happ e and Frith stimulated my own thinking about social

developmental neuroscience and about the future of this discipline.

When and why does development go awry? Those interested in atypical development must address several pressing issues. The first is the perplexing notion of how similar early experiences or genetic variations can lead to very different developmental outcomes. At a coarse level, for example, why does one child develop autism and another schizophrenia, given the reported overlap in genes? At a finer level, why do two children with similar genetic risk and seemingly identical rearing conditions (i.e., siblings of an older child with autism) develop differently? Clearly, there are perturbations in brain development that presumably occur early that lead one child down one pathway and another down another pathway, but our understanding of which developmental trajectory a child follows is extraordinarily limited. Autism, for example, is a disorder that generally makes its appearance in the second to third year of life and whose elements can be identified in high risk populations much earlier. Yet, we still do not understand precisely when brain development has gone awry to lead to autism, nor what specifically has gone awry. A similar conundrum applies to the principle of equifinality in atypical development. There are several different populations of children at elevated risk for developing autism (note that the prevalence of autism in the general population is approximately 1%). For example, the prevalence of autism among children who have grown up in institutions is roughly 5%–10%; the figure is 20% among children with an older sibling with autism, 60% among those with Tuberous Sclerosis Complex, 5%– 10% among children with Down Syndrome, and 10%–20% among those with Duchenne Muscular Dystrophy. These are all extraordinarily different disorders, yet a sizeable percentage of children afflicted with these disorders develop autism. Of course, whether they have the same type of autism is unknown, but clearly the phenotype is similar despite what are thought to be very different underlying mechanisms. A final question is when precisely brain development goes awry to lead, eventually, to a derailing of

© 2014 The Authors. Journal of Child Psychology and Psychiatry. © 2014 Association for Child and Adolescent Mental Health. Published by John Wiley & Sons Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main St, Malden, MA 02148, USA

doi:10.1111/jcpp.12254

development. For example, it is generally assumed that disorders that appear in the first years of life likely reflect errors in brain development that occur close in time to their onset. However, schizophrenia is a disorder that often does not appear until late adolescence or early adulthood, yet most agree it reflects a disruption in brain development that occurs in the 2nd or 3rd trimester of pregnancy – why, then, does it not manifest itself earlier? And, if we were able to examine the fine architecture of the brain of the newborn, would we be able to tell the difference between the brain that will develop autism and the one that will develop schizophrenia?

Innate versus learned – the role of experience versus pre-preprogramming Another critical challenge for those studying development is investigating the contributions of experience versus biological preparedness to the emergence of core abilities. There are still many in the field of psychology who use the term ‘innate’ too loosely and often incorrectly. For example, in a recent book, Bloom (2013) argues that infants have an ‘innate’ moral sense; similarly, Spelke, Carey, Baillargeon, Wynn, and others have argued that select aspects of early cognitive development are ‘innate’ (e.g., elements of number concept, of object concept, etc.). In my view, the term ‘innate’ as applied to highly complex behaviors (e.g., morality) is likely misguided in at least two ways. First, simply because an ability appears early in life or appears in a variety of cultures does not mean it is innate qua innate. For instance, as Happ e and Frith correctly note, newborns prefer face-like stimuli over nonface-like stimuli; however, such preferences could very well be due to a rapid learning mechanism that takes place over the first minutes and hours after birth, when faces are ubiquitous in the infant’s environment. Second, noticeably lacking from most nativist arguments is any appreciation of the genetic and/or neurobiological underpinnings of the behavior in question. Thus, for example, if even a rudimentary sense of right and wrong, just and unjust, etc. reflects the activity of multiple neural circuits distributed widely in the brain, surely these circuits are largely dependent on experiential inputs for their formation and elaboration; it is inconceivable that with only 20,000 genes in our genome that so many genes would be dedicated to building such elaborate circuitry. Here, Greenough’s notion of experience-expectant development is very helpful, as it argues that the young infant need only possess rudimentary brain architecture early in life, architecture that will become more elaborate and in some cases, specialized, based on experiences common to most members of the species (e.g., patterned light, speech, adequate caregiving, etc.; see Greenough & Black, 1992).

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Sensitive periods The role of experiential inputs during sensitive periods in shaping atypical developmental trajectories is another critical issue that merits consideration. There is extensive evidence from rodents, monkeys, and humans that many aspects of early social behavior depend on experiences occurring during a critical period of development. We know from studies of psychosocial deprivation, for example, that attachment behavior is seriously and perhaps permanently altered if access to species-typical caregiving is lacking early in life (see Nelson, Fox, & Zeanah, 2014). Similarly, we know the processing of facial identity and facial emotion can be altered by perturbations in early experience. Together, these findings raise a critical question for the study of atypical social development. Specifically, if many aspects of social development are experience-expectant or experience-dependent (see Greenough & Black, 1992, for elaboration), does that imply that the deficits in social behavior (e.g., social communication; social relatedness) are due to a failure to incorporate such experiences, and if so, why? I offer a few possible scenarios. First, we must consider the possibility that the neural architecture that would normally underpin certain social behaviors is somehow compromised early in life, and as a result, is unable to benefit from experience in the way a typically developing brain might. Of course, a problem with this approach is that it implies a lack of plasticity. For example, we know that the brains of children born with focal lesions in speech/language areas (e.g., due to stroke) will most often compensate and recruit other regions, leading to reasonably normal language development. Given the intractability of the deficits in social behavior commonly observed in children with a variety of neurodevelopmental disorders (e.g., autism, reactive attachment disorder), does this imply a lack of plasticity in associated neural systems, and if so, why is social behavior different from, say, language? An alternative view is that the underlying neural architecture is intact but that there is an error in neurochemistry; thus, for example, perhaps the dopaminergic-reward system is altered in children with autism, which leads them to attend little to faces (or fail to scan faces in a typical fashion) because either faces do not activate the reward system (whereas perhaps inanimate objects do) or because such children find faces aversive and go out of their way to avoid them. Of course, in both cases, the end result is the same – inattention to faces – making it difficult to ascertain which of these two possible underlying mechanisms is to blame. A final possibility is that higher level social behaviors, such as theory of mind, are dependent on more elementary core social constructs. If the development of these elementary ‘building blocks’, has been altered or corrupted early in life, this might

© 2014 The Authors. Journal of Child Psychology and Psychiatry. © 2014 Association for Child and Adolescent Mental Health.

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Charles A. Nelson

contribute to higher-order social cognitive and behavioral deficits. Thus, for example, if infants do not find looking at faces rewarding, then parent– infant interactions can be altered, which in turn might lead to deficits in social communication. Similarly, if the mirror neuron system has been corrupted early in development, then infants may fail to imitate. And, if both of these fundamental building blocks are altered, infants may develop what Baron-Cohen has referred to as ‘mind blindness’ (i.e., the ability to understand how another person feels or thinks about an issue). Of course, this is all speculation on my part but my point is simply that it is essential that we understand the role of experience in regulating both typical and atypical social development.

‘Lumps’ of tissue versus neural networks Much of what we know about brain-behavior associations in social behavior (and cognition, as well) is based on correlations obtained in various neuroimaging tasks or in postmortem studies. For example, there are long-established associations between the hippocampus and memory, between the amygdala and emotion, between the fusiform gyrus and face processing, between Broca’s area and speech, and so on. But, is this really how the brain works? Does the hippocampus really ‘do’ memory? Does the amygdala really ‘do’ emotion? Surely this view, which dates back to the 19th century, is simplistic at best. We know that brain function depends on neural circuitry, that the balance between excitation and inhibition of neural circuits influences circuit function, and that most functions depend on highly complex and distributed circuits. I would argue that if we understand how circuits are built in the typically developing brain, we would be in a better position to understand so-called ‘connectopathies’. Of course, the reverse may also hold true: by studying errors in circuit formation we may be in a better position to understand what normal circuits do and how they develop. My point, though, is that we need to move beyond the phrenology approach to brain-behavior associations and embrace a more contemporary view of how brains are built over time.

Methodological issues An issue at the very heart of our ability to elucidate the relation between brain development and social behavior concerns methods. Three approaches have historically been adopted in this context. The first is to visualize the brain at work, ideally in the context of a child performing a specific task (e.g., what areas of the brain are activated during a theory of mind task?). An alternative approach is to examine function–structure associations by, for example, performing an MRI on a child who is subsequently

J Child Psychol Psychiatr 2014; 55(6): 578–81

evaluated behaviorally (e.g., what is the correlation between cortical thinning over prefrontal cortex and emotion regulation?). A third approach, generally adopted with clinical populations, is to examine the association between a particular lesion in the brain and its corresponding effects on behavior (e.g., what effect does a lesion of the amygdala have on recognizing fearful emotions?). Each approach has its advantages and disadvantages. Visualizing the brain during the performance of some task may represent the ideal, as it allows a tighter temporal coupling between brain and behavior. Alas, several disadvantages should also be noted. First, neuroimaging tools vary in their ability to resolve space and time, and as a result, some tools are better at elucidating ‘where’ in the brain activity is taking place and others are better at tracking the moment-by-moment transactions taking place during the performance of some task. Second, not all tools can be used at all ages; for example, fMRI, which has very good spatial resolution, is exceedingly limited in its utility in the first years of life, simply because infants must generally be asleep during testing in order to lie still enough to obtain good data, and a sleeping infant limits the kinds of tasks that can be performed. A disadvantage to examining structure–function relations is the imperfect coupling between the two; for example, some children who are born without a corpus callosum experience few if any development and learning challenges, and some children who have their left hemisphere removed early in life (due to intractable seizures) may develop reasonably normal language. Finally, although the lesion approach has been used for at least two centuries, it is limited in what it tells us about groups of individuals versus a specific individual; it also tells us little about plasticity.

Next steps in improving our knowledge of social and brain development Despite the methodological caveats described above, the future of developmental social neuroscience looks bright. First, advanced analytics have greatly improved what can be extracted from all manner of imaging data. Second, faster sequences, higher field strength magnets, and denser head coils have shortened the time a child must lie still in a MRI scanner and also improve spatial resolution. Third, the use of functional Near Infrared Spectroscopy (fNIRS) enables examination of brain metabolism in an awake, behaving, and, in some cases, mobile young child. Fourth, many of these tools have been used alongside eye tracking technology, which has provided greater specificity about underlying neural circuitry (e.g., instead of examining the face region of the brain generally, it is now possible to examine the neural correlates of scanning the eyes, the mouth, etc.). Fifth, the advent of imaging genetics

© 2014 The Authors. Journal of Child Psychology and Psychiatry. © 2014 Association for Child and Adolescent Mental Health.

doi:10.1111/jcpp.12254

offers the potential to better leverage individual differences, an often overlooked but vital area of inquiry. Finally, animal models of social behavior have substantially improved our knowledge of both the neurobiology and molecular genetics of social development. The Happ e and Frith article represents an important next step in our ability to understand the association between brain development and the development of social behavior; moreover, it does so in the context of shedding light on both typical and atypical development. It is my hope that the conceptual framework provided by the authors will inspire current and future generations of scientists to forge new inroads into this important area of human development.

Acknowledgements This commentary article was invited by the JCPP Editor-in-Chief and has been subject to internal review. The writing of this article was made possible by grants from the National Institutes of Health (MH078829, MH091363, DC010290). The author declares that he has no competing or potential conflicts of interest in relation to this article. The author thanks

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Cora Mukerji for comments on an earlier draft of this manuscript.

Correspondence Charles Nelson, Children’s Hospital Boston, Developmental Medicine Research. 1 Autumn Street, Office AU621, Mailbox #713, Boston, MA 02115-5365, USA; Email: [email protected]

References Bloom, P. (2013). Just babies: the origins of good and evil. New York: Crown Publishers. Greenough, W.T., & Black, J.E. (1992). Induction of brain structure by experience: substrates for cognitive development. In M.R. Gunnar & C.A. Nelson (Eds.), The Minnesota symposia on child psychology Vol. 24: Developmental behavioral (pp. 155– 200). Mahwah, NJ: Lawrence Earlbaum. Happ e, F., & Frith, U. (2014). Annual Research Review: Towards a developmental neuroscience of atypical social cognition. Journal of Child Psychology and Psychiatry, 55, 553–577. Nelson, C.A., Fox, N.A., & Zeanah, C.H. (2014). Romania’s abandoned children: Deprivation, brain development and the struggle for recovery. Cambridge, MA: Harvard University Press.

Accepted for publication: 9 January 2014

© 2014 The Authors. Journal of Child Psychology and Psychiatry. © 2014 Association for Child and Adolescent Mental Health.

Commentary: Becoming social--a commentary on Happé & Frith (2014).

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