Greater functional connectivity between sensory networks is related to symptom severity in toddlers with autism spectrum disorder

Abstract

Background Symptoms of autism spectrum disorder (ASD) emerge in the first years of life. Yet, little is known about the organization and development of functional brain networks in ASD proximally to the symptom onset. Further, the relationship between brain network connectivity and emerging ASD symptoms and overall functioning in early childhood is not well understood. Methods Resting‐state fMRI data were acquired during natural sleep from 24 young children with ASD and 23 typically developing (TD) children, aged 17–45 months. Intrinsic functional connectivity (iFC) within and between resting‐state functional networks was derived with independent component analysis (ICA). Results Increased iFC between visual and sensorimotor networks was found in young children with ASD compared to TD participants. Within the ASD group, the degree of overconnectivity between visual and sensorimotor networks was associated with greater autism symptoms. Age‐related weakening of the visual–auditory between‐network connectivity was observed in the ASD but not the TD group. Conclusions Taken together, these results provide evidence for disrupted functional network maturation and differentiation, particularly involving visual and sensorimotor networks, during the first years of life in ASD. The observed pattern of greater visual–sensorimotor between‐network connectivity associated with poorer clinical outcomes suggests that disruptions in multisensory brain circuitry may play a critical role for early development of behavioral skills and autism symptomatology in young children with ASD.

Atypical core-periphery brain dynamics in autism

“…This result from localization analysis suggests that the somatosensory network drives, at least in part, the increase in modularity across time seen in neurotypicals relative to those with ASD (Harlalka et al, 2018 ; Henry et al, 2018 ). In a recent study, it was further demonstrated in toddlers with ASD that the degree of overconnectivity between visual and sensorimotor networks was associated with greater autism symptoms, and an age-related weakening of the visual-auditory between-network connectivity was observed in the ASD but not the TD group (B. Chen et al, 2020 ).…”

“…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 ASD (Ciarrusta et al, 2019 ). Furthermore, stronger functional connectivity and the degree of overconnectivity between visual and sensorimotor networks were associated with greater autism symptoms in toddlers (B. Chen et al, 2020 ; Ciarrusta et al, 2019 ).…”

“…In spite of site-specific heterogeneity and inclusion of nonoverlapping samples in the studies listed in Table 2 from the Autism Brain Imaging Data Exchange (ABIDE), there is increasing convergence in support of a developmental model accounting for the age-specific over- and underconnectivity findings in ASD. This model posits that childhood autism is characterized by brain hyperconnectivity, whereas adolescent and adulthood autism is characterized by brain hypoconnectivity (B. Chen et al, 2020 ; Delmonte et al, 2013 ; Guo et al, 2017 ; Guo et al, 2019 ; Harlalka et al, 2018 ; Henry et al, 2018 ; Huang et al, 2015 ; Nomi & Uddin, 2015 ). These findings suggest atypical cortical developmental trajectories across the life span, and highlight the importance of taking different developmental stages into account when exploring the potential neural mechanisms of ASD (Gollo et al, 2017 ; Hahamy et al, 2015 ; Henry et al, 2018 ; Naik, Banerjee, Bapi, Deco, & Roy, 2017 ; Naik, Subbareddy, Banerjee, Roy, & Bapi, 2017 ).…”

“…However, complementary to the above findings, it was also observed that there was an overall idiosyncratic pattern distributed over the whole brain in adults with ASD, with a lack of segregation of functional networks and a higher integration of the component regions of interest in ASD (Hahamy et al, 2015 ). Thus, hypoconnectivity within networks may partially be explained by a lack of differentiation in adulthood and increased connectivity within sensory areas (B. Chen et al, 2020 ).…”

“…Several studies showed decreased functional connectivity among cortical regions associated with social functions, such as the superior temporal sulcus, medial prefrontal, temporoparietal junction, left inferior frontal gyrus, as well as somatosensory cortex (Alaerts et al, 2015 ; Alaerts et al, 2014 ; Anderson et al, 2011 ; Baum et al, 2017 ), with some showing simultaneously increased functional connectivity between thalamus, striatum, and some of the same cortical regions (Abbott et al, 2018 ; Alaerts et al, 2015 ; Anderson et al, 2011 ; Cerliani et al, 2015 ; but see Nair et al, 2013 ). Findings from the task-based functional magnetic resonance imaging literature demonstrate that the above subcortical and cortical brain regions are involved in restricted and repetitive behaviors (RRB) and may represent some of the earliest biomarkers of ASD (B. Chen et al, 2020 ; Ciarrusta et al, 2019 ; Robertson & Baron-Cohen, 2017 ). Previous studies also reported that individuals with autism showed increased functional connectivity between regions in the frontal cortex (anterior cingulate cortex, ACC; middle frontal gyrus, MFG; paracingulate gyrus, Pcg; and orbitofrontal cortex, OFC), and striatum (nucleus accumbens, NAcc; and caudate) compared with neurotypical individuals (Abbott et al, 2018 ; Cerliani et al, 2015 ; Delmonte et al, 2013 ; Jasmin et al, 2019 ).…”