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- Title
Social Brain Functional Maturation in Newborn Infants With and Without a Family History of Autism Spectrum Disorder.
- Authors
Ciarrusta, Judit; O'Muircheartaigh, Jonathan; Dimitrova, Ralica; Batalle, Dafnis; Cordero-Grande, Lucilio; Price, Anthony; Hughes, Emer; Steinweg, Johannes Klaus; Kangas, Johanna; Perry, Emily; Javed, Ayesha; Stoencheva, Vladimira; Akolekar, Ranjit; Victor, Suresh; Hajnal, Joseph; Murphy, Declan; Edwards, David; Arichi, Tomoki; McAlonan, Grainne
- Abstract
Key Points: Question: Are changes in the maturation of the social brain in infants associated with vulnerability to neurodevelopmental conditions such as autism spectrum disorder? Findings: In this cohort study of 36 neonates with and without a family history of autism spectrum disorder, newborns with a family history of autism spectrum disorder had significantly higher neural activity in the right fusiform and left parietal cortex. In addition, the pattern of age-related changes in spontaneous activity in the cingulate and insula was disrupted in infants with a family history of autism spectrum disorder. Meaning: Atypical development of functional activity patterns in key regions responsible for social processing may be a vulnerability mechanism for autism. This cohort study compares functional magnetic resonance imaging of the brains of neonates with a family history of autism spectrum disorder (ASD) vs those of neonates with no family history of ASD. Importance: 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. Objective: To assess whether alternation of functional maturation of social brain circuits is associated with a family history of ASD in newborns. Design, Setting, and Participants: 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. Main Outcomes and Measures: 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. Results: 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. Conclusions and Relevance: 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.
- Subjects
ENGLAND; MAGNETIC resonance imaging equipment; AGE distribution; AUTISM; BRAIN; COMPARATIVE studies; GESTATIONAL age; INFANT development; LONGITUDINAL method; RESEARCH funding; SOCIAL skills; EXTENDED families; CONTENT mining; FAMILY history (Medicine); DESCRIPTIVE statistics; CHILDREN
- Publication
JAMA Network Open, 2019, Vol 2, Issue 4, pe191868
- ISSN
2574-3805
- Publication type
Article
- DOI
10.1001/jamanetworkopen.2019.1868