Joint Attention and Brain Functional Connectivity in Infants and Toddlers Cerebral Cortex

Initiating joint attention (IJA), the behavioral instigation of coordinated focus of 2 people on an object, emerges over the first 2 years of life and supports social-communicative functioning related to the healthy development of aspects of language, empathy, and theory of mind. Deficits in IJA provide strong early indicators for autism spectrum disorder, and therapies targeting joint attention have shown tremendous promise. However, the brain systems underlying IJA in early childhood are poorly understood, due in part to significant methodological challenges in imaging localized brain function that supports social behaviors during the first 2 years of life. Herein, we show that the functional organization of the brain is intimately related to the emergence of IJA using functional connectivity magnetic resonance imaging and dimensional behavioral assessments in a large semilongitudinal cohort of infants and toddlers. In particular, though functional connections spanning the brain are involved in IJA, the strongest brain-behavior associations cluster within connections between a small subset of functional brain networks; namely between the visual network and dorsal attention network and between the visual network and posterior cingulate aspects of the default mode network. These observations mark the earliest known description of how functional brain systems underlie a burgeoning fundamental social behavior, may help improve the design of targeted therapies for neurodevelopmental disorders, and, more generally, elucidate physiological mechanisms essential to healthy social behavior development. The emergence of joint attention (JA), the coordinated orienting of 2 people toward an object or event, occurs during the first 2 years of life, arguably the most dynamic and important period of early child development (Scaife and Bruner 1975). It is theorized that engaging in JA lays the foundation for prosocial cooperative behavior, from basic social-communicative functioning and language development (Premack 2004) to sophisticated forms of empathy (Mundy and Jarrold 2010) and theory of mind (Adolphs 2003). In fact, early exhibition of joint attention is strongly associated with later language ability (Morales et al. 2000; Mundy et al. 2007), and atypical development of the initiation of joint attention (IJA) is strongly indicative of autism spectrum disorder (ASD) (Bruinsma et al. 2004). The neural substrates underlying IJA in early childhood are poorly understood (Barak and Feng 2016), due in part to significant methodological challenges in imaging localized brain function that supports social behaviors in children during the first 2 years of life.