Abstract
What is inherited or acquired in neurodevelopmental conditions such as autism spectrum disorder (ASD) is not a fixed outcome, but instead is a vulnerability to a spectrum of traits, especially social difficulties. Identifying the biological mechanisms associated with vulnerability requires looking as early in life as possible, before the brain is shaped by postnatal mechanisms and/or the experiences of living with these traits. Animal studies suggest that susceptibility to neurodevelopmental disorders arises when genetic and/or environmental risks for these conditions alter patterns of synchronous brain activity in the perinatal period, but this has never been examined in human neonates. To assess whether alternation of functional maturation of social brain circuits is associated with a family history of ASD in newborns. In this cohort study of 36 neonates with and without a family history of ASD, neonates underwent magnetic resonance imaging at St Thomas Hospital in London, England, using a dedicated neonatal brain imaging system between June 23, 2015, and August 1, 2018. Neonates with a first-degree relative with ASD (R+) and therefore vulnerable to autistic traits and neonates without a family history (R-) were recruited for the study. Synchronous neural activity in brain regions linked to social function was compared. Regions responsible for social function were selected with reference to a published meta-analysis and the level of synchronous activity within each region was used as a measure of local functional connectivity in a regional homogeneity analysis. Group differences, controlling for sex, age at birth, age at scan, and group × age interactions, were examined. The final data set consisted of 18 R+ infants (13 male; median [range] postmenstrual age at scan, 42.93 [40.00-44.86] weeks) and 18 R- infants (13 male; median [range] postmenstrual age at scan, 42.50 [39.29-44.58] weeks). Neonates who were R+ had significantly higher levels of synchronous activity in the right posterior fusiform (t = 2.48; P = .04) and left parietal cortices (t = 3.96; P = .04). In addition, there was a significant group × age interaction within the anterior segment of the left insula (t = 3.03; P = .04) and cingulate cortices (right anterior: t = 3.00; P = .03; left anterior: t = 2.81; P = .03; right posterior: t = 2.77; P = .03; left posterior: t = 2.55; P = .03). In R+ infants, levels of synchronous activity decreased over 39 to 45 weeks' postmenstrual age, whereas synchronous activity levels increased in R- infants over the same period. Synchronous activity is required during maturation of functionally connected networks. This study found that in newborn humans, having a first-degree relative with ASD was associated with higher levels of local functional connectivity and dysmaturation of interconnected regions responsible for processing higher-order social information.
Highlights
Social cognition refers to “the ability to perceive and process information from others, from one’s self and interpersonal knowledge.”[1]
This study found that in newborn humans, having a first-degree relative with autism spectrum disorder (ASD) was associated with higher levels of local functional connectivity and dysmaturation of interconnected regions responsible for processing higher-order social information
Main Effect on Synchronous Activity The final data set consisted of 18 R+ infants (13 male; median [range] postmenstrual age at scan, 42.93 [40.00-44.86] weeks) and 18 R− infants (13 male; median [range] postmenstrual age at scan, 42.50 [39.29-44.58] weeks)
Summary
Social cognition refers to “the ability to perceive and process information from others, from one’s self and interpersonal knowledge.”[1] The human brain has evolved to become more highly specialized in social interaction and communication than brains of any other species.[2] This ability starts maturing early in life and quickly becomes highly complex through building on fundamental processes such as basic sensory integration and emotion recognition.[3] Later in development, social function incorporates higher-order processes, such as mental state attribution, involving integrated activity in several regions across the whole brain These regions make up the “social brain,” which has recently been defined by a meta-analysis of neuroimaging studies in social neuroscience as comprising 36 distinct regions. ASD deficits in processing facial features have been associated with altered connectivity in the fusiform gyrus,[6,7] difficulty with social demands has been associated with poor connectivity in the cingulate cortex,[8] and aberrant processing of social stimuli has been associated with atypical activation patterns in the insula.[9]
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