Response patterns in the developing social brain are organized by social and emotion features and disrupted in children diagnosed with autism spectrum disorder

Abstract

Adults and children recruit a specific network of brain regions when engaged in "Theory of Mind" (ToM) reasoning. Recently, fMRI studies of adults have used multivariate analyses to provide a deeper characterization of responses in these regions. These analyses characterize representational distinctions within the social domain, rather than comparing responses across preferred (social) and non-preferred stimuli. Here, we conducted opportunistic multivariate analyses in two previously collected datasets (Experiment 1: n=20 5-11 year old children and n=37 adults; Experiment 2: n=76 neurotypical and n=29 5-12 year old children diagnosed with Autism Spectrum Disorder (ASD)) in order to characterize the structure of representations in the developing social brain, and in order to discover if this structure is disrupted in ASD. Children listened to stories that described characters' mental states (Mental), non-mentalistic social information (Social), and causal events in the environment (Physical), while undergoing fMRI. We measured the extent to which neural responses in ToM brain regions were organized according to two ToM-relevant models: 1) a condition model, which reflected the experimentergenerated condition labels, and 2) a data-driven emotion model, which organized stimuli according to their emotion content. We additionally constructed two control models based on linguistic and narrative features of the stories. In both experiments, the two ToM-relevant models outperformed the control models. The fit of the condition model increased with age in neurotypical children. Moreover, the fit of the condition model to neural response patterns was reduced in the RTPJ in children diagnosed with ASD. These results provide a first glimpse into the conceptual structure of information in ToM brain regions in childhood, and suggest that there are real, stable features that predict responses in these regions in children. Multivariate analyses are a promising approach for sensitively measuring conceptual and neural developmental change and individual differences in ToM.

Neural similarity between mentalizing and live social interaction during the transition to adolescence

“…Starting in early childhood, individuals' peer relationships become increasingly important, such that they spend progressively more time with friends over parents, and this social re‐orienting is accompanied by changes in brain systems associated with perception, motivation/affect, and executive function (Ladd, 1999 ; Nelson et al, 2016 ; Parker et al, 2006 ). This trajectory aligns with neuroimaging work demonstrating that the mentalizing network is functionally distinct by the age of three (Richardson et al, 2018 ), but exhibits increasing functional specialization through adolescence and into adulthood (Gweon et al, 2012 ; Moraczewski et al, 2020 ; Richardson et al, 2020 ). There is also increased sensitivity in the brain's reward system to social contexts as children transition into adolescence (Chein et al, 2011 ; Moreira & Telzer, 2018 ; Smith et al, 2015 ), and activity in the reward and mentalizing networks during adolescence is indicative of a tendency to spontaneously integrate peer perspectives into self‐evaluations (Jankowski et al, 2014 ; Pfeifer et al, 2009 ; Van der Cruijsen et al, 2019 ).…”

A size‐adaptive 32‐channel array coil for awake infant neuroimaging at 3 Tesla MRI

“…As we have shown in previous pediatric brain studies, 5,10,31,32 a dedicatedly designed tight‐fitting array coil for the pediatric population provides substantial SNR benefits over adult head coils. Our constructed adjustable array coil shows similar results.…”

The representation of mental state information in schizophrenia and first-degree relatives: a multivariate pattern analysis of fMRI data

“…, 2009 ; Koster-Hale et al. , 2013 ; Richardson et al. , 2020 ), suggesting that altered representation of mental state information may be a transdiagnostic marker of social dysfunction.…”

“…, 2011 ; Koster-Hale et al. , 2013 ; Richardson et al. , 2020 ), and the ToM network more generally ( Skerry and Saxe, 2015 ; Tamir et al.…”