Reduced Gyrification Is Related to Reduced Interhemispheric Connectivity in Autism Spectrum Disorders

Abstract

Objective. Autism spectrum disorders (ASD) have been associated with atypical cortical grey and subcortical white matter development. Neurodevelopmental theories postulate that a relation between cortical maturation and structural brain connectivity may exist. We therefore investigated the development of gyrification and white matter connectivity and their relationship in individuals with ASD and their typically developing peers.Method. T1-and diffusion-weighted images were acquired from a representative sample of 30 children and adolescents with ASD (aged 8 to 18 years), and 29 typically developing children matched for age, sex, hand preference, and socioeconomic status. The FreeSurfer suite was used to calculate cortical volume, surface area, and gyrification index. Measures of structural connectivity were estimated using probabilistic tractography and tract-based spatial statistics (TBSS).Results. Left prefrontal and parietal cortex showed a relative, age-dependent decrease in gyrification index in children and adolescents with ASD compared to typically developing controls. This result was replicated in an age and IQ-matched sample provided by the Autism Brain Imaging Data Exchange (ABIDE) initiative. Furthermore, tractography and TBSS showed a complementary pattern, where left prefrontal gyrification was negatively related to radial diffusivity in the forceps minor in participants with ASD.Conclusion. The present study builds on earlier findings of abnormal gyrification and structural connectivity in the prefrontal cortex in ASD. It provides a more comprehensive neurodevelopmental characterization of ASD, involving interdependent changes in microstructural white and cortical grey matter. The findings of related abnormal patterns of gyrification and white matter connectivity support the notion of the intertwined development of two major morphometric domains in ASD.

Early patterns of functional brain development associated with autism spectrum disorder in tuberous sclerosis complex

“…S2). In nonsyndromic ASD, several neurobiological mechanisms have been attributed to underlie the atypical "crossover" trajectory captured in ASD, including differences in axonal pruning and myelination [Wolff et al, 2015;Wolff et al, 2012], differences in large scale anatomy [Courchesne, 2004;Hazlett et al, 2017], and a complex interplay between gray and white matter changes [Bos et al, 2015;Ecker et al, 2016]. It should be noted that this is the first study to examine such change in neural function in TSC, and it supports the need for longitudinal investigation in neurodevelopmental disorders, regardless of underlying genetic etiology.…”

Early patterns of functional brain development associated with autism spectrum disorder in tuberous sclerosis complex

“…Therefore, it is possible that the lack of significant connectivity differences at 12 months may reflect a transitional period in the infants who go on to develop ASD (see figure 3). In nonsyndromic ASD, several neurobiological mechanisms have been attributed to underlie the atypical 'crossover' trajectory captured in ASD, including differences in axonal pruning and myelination (Wolff et al, 2015(Wolff et al, , 2012, differences in large scale anatomy (Courchesne, 2004;Hazlett et al, 2017), and a complex interplay between gray and white matter changes (Bos et al, 2015;Ecker et al, 2016). It should be noted that this is the first study to examine such change in neural function in TSC, and it supports the need for longitudinal investigation in neurodevelopmental disorders, regardless of underlying genetic etiology.…”

Adolescent maturation of the relationship between cortical gyrification and cognitive ability

“…This offers the possibility that frontoparietal gyrification decreases in adolescence are one of several brain structure changes that reflect more efficient, firmly established, and mature distributed neural networks. This idea is largely speculative at this point, because only a few clinical studies have directly examined the relationships between local gyrification covariance and structural connectivity as measured by functional neuroimaging (Bos et al, 2015; Schaer et al, 2013). For example, reduced left prefrontal gyrification in children and adolescents with autism spectrum disorders (ages 8–18 years) was related to reduced inter-hemispheric structural connectivity (Bos et al, 2015).…”

“…This idea is largely speculative at this point, because only a few clinical studies have directly examined the relationships between local gyrification covariance and structural connectivity as measured by functional neuroimaging (Bos et al, 2015; Schaer et al, 2013). For example, reduced left prefrontal gyrification in children and adolescents with autism spectrum disorders (ages 8–18 years) was related to reduced inter-hemispheric structural connectivity (Bos et al, 2015). Future studies should directly examine the relationship between cortical folding and functional connectivity developmental changes in adolescence.…”