Children with autism spectrum disorder show altered functional connectivity and abnormal maturation trajectories in response to inverted faces

Mamashli, Fahimeh; Kozhemiako, Nataliia; Khan, Sheraz; Nunes, Adonay S.; McGuiggan, Nicole M.; Losh, Ainsley; Joseph, Robert M.; Ahveninen, Jyrki; Doesburg, Sam M.; Hämäläinen, Matti S.; Kenet, Tal

doi:10.1002/aur.2497

Cited by 14 publications

(14 citation statements)

References 85 publications

(138 reference statements)

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“…In contrast, the only disorder on the list that is considered neurodevelopmental, i.e., early origin, autism, showed age-dependent resilience only in the gamma band. This suggests that beta band networks might not undergo normal development in autism during adolescence, and thus are particularly or more severely impacted in line with prior findings ( 12 , 22 , 76 , 77 ). Anxiety was the only term that corresponded to networks showing age-dependent trajectories in both the beta and gamma bands differentiating it from the other tested terms.…”

Section: Discussionsupporting

confidence: 87%

Functional Significance of Human Resting-State Networks Hubs Identified Using MEG During the Transition From Childhood to Adulthood

et al. 2022

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Cortical hubs identified within resting-state networks (RSNs), areas of the cortex that have a higher-than-average number of connections, are known to be critical to typical cognitive functioning and are often implicated in disorders leading to abnormal cognitive functioning. Functionally defined cortical hubs are also known to change with age in the developing, maturing brain, mostly based on studies carried out using fMRI. We have recently used magnetoencephalography (MEG) to study the maturation trajectories of RSNs and their hubs from age 7 to 29 in 131 healthy participants with high temporal resolution. We found that maturation trajectories diverge as a function of the underlying cortical rhythm. Specifically, we found the beta band (13–30 Hz)-mediated RSNs became more locally efficient with maturation, i.e., more organized into clusters and connected with nearby regions, while gamma (31–80 Hz)-mediated RSNs became more globally efficient with maturation, i.e., prioritizing faster signal transmission between distant cortical regions. We also found that different sets of hubs were associated with each of these networks. To better understand the functional significance of this divergence, we wanted to examine the cortical functions associated with the identified hubs that grew or shrunk with maturation within each of these networks. To that end, we analyzed the results of the prior study using Neurosynth, a platform for large-scale, automated synthesis of fMRI data that links brain coordinates with their probabilistically associated terms. By mapping the Neurosynth terms associated with each of these hubs, we found that maturing hubs identified in the gamma band RSNs were more likely to be associated with bottom-up processes while maturing hubs identified in the beta band RSNs were more likely to be associated with top-down functions. The results were consistent with the idea that beta band-mediated networks preferentially support the maturation of top-down processing, while the gamma band-mediated networks preferentially support the maturation of bottom-up processing.

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Section: Discussionsupporting

confidence: 87%

Functional Significance of Human Resting-State Networks Hubs Identified Using MEG During the Transition From Childhood to Adulthood

et al. 2022

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“…The authors showed that during somatosensory stimulation, ASD participants were characterized by the presence of increased long-range feed-forward connectivity from the primary (S1) to secondary (S2) somatosensory cortex at 25 Hz (i.e., beta band), and this strengthened connectivity was correlated with multisensory processing abnormalities. Complementarily, the ASD participants were characterized by reduced long-range feedback connectivity [ 26 ]. The weakness in top-down signaling in ASD was confirmed by Seymour et al [ 27 ] using a visual task: V4-to-V1 feedback connectivity in the alpha band was reduced in individuals on the autism spectrum compared to healthy controls and the strength of this feedback connectivity was inversely related to the autistic quotient score.…”

Section: Introductionmentioning

confidence: 99%

The Directionality of Fronto-Posterior Brain Connectivity Is Associated with the Degree of Individual Autistic Traits

et al. 2021

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Altered patterns of brain connectivity have been found in autism spectrum disorder (ASD) and associated with specific symptoms and behavioral features. Growing evidence suggests that the autistic peculiarities are not confined to the clinical population but extend along a continuum between healthy and maladaptive conditions. The aim of this study was to investigate whether a differentiated connectivity pattern could also be tracked along the continuum of autistic traits in a non-clinical population. A Granger causality analysis conducted on a resting-state EEG recording showed that connectivity along the posterior-frontal gradient is sensitive to the magnitude of individual autistic traits and mostly conveyed through fast oscillatory activity. Specifically, participants with higher autistic traits were characterized by a prevalence of ascending connections starting from posterior regions ramping the cortical hierarchy. These findings point to the presence of a tendency within the neural mapping of individuals with higher autistic features in conveying proportionally more bottom-up information. This pattern of findings mimics those found in clinical forms of autism, supporting the idea of a neurobiological continuum between autistic traits and ASD.

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“…In addition, our paradigm, which consists of the administration of OT, imaging sessions, and performance tasks, has led to long and complex meetings. Although the size of our sample is equivalent to the sample sizes from other studies with similar experimental designs [ 27 , 29 ], given the complexity of the electrophysiology analyses and the neural variability that exists between individuals, we encourage follow-up studies to examine the effects of OT on early attentional processes on a more extensive and heterogenic sample in terms of gender, age, and clinical characteristics. Our sample size can also explain the lack of correlation between OT effects and the age or clinical assessment of the participants.…”

Section: Discussionmentioning

confidence: 99%

“…During social perception, PAC can shed more light on the balance between top-down and bottom-up perception in ASD by examining the relationships between low and high frequencies. Indeed, studies have shown that individuals with ASD present reduced coupling during face perception in ASD for both long- and short-range connectivity, a reduction that was correlated with clinical symptoms severity [ 40 , 27 ].…”

Section: Introductionmentioning

confidence: 99%

Oxytocin impacts top-down and bottom-up social perception in adolescents with ASD: a MEG study of neural connectivity

2022

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Background In the last decade, accumulative evidence has shown that oxytocin can modulate social perception in typically developed individuals and individuals diagnosed with autism. While several studies show that oxytocin (OT) modulates neural activation in social-related neural regions, the mechanism that underlies OT effects in ASD is not fully known yet. Despite evidence from animal studies on connections between the oxytocinergic system and excitation/inhibition neural balance, the influence of OT on oscillatory responses among individuals with ASD has been rarely examined. To bridge these gaps in knowledge, we investigated the effects of OT on both social and non-social stimuli while focusing on its specific influence on the neural connectivity between three socially related neural regions—the left and right fusiform and the medial frontal cortex. Methods Twenty-five adolescents with ASD participated in a wall-established social task during a randomized, double-blind placebo-controlled MEG and OT administration study. Our main task was a social-related task that required the identification of social and non-social-related pictures. We hypothesized that OT would modulate the oscillatory connectivity between three pre-selected regions of interest to be more adaptive to social processing. Specifically, we focused on alpha and gamma bands which are known to play an important role in face processing and top-down/bottom-up balance. Results Compared to placebo, OT reduced the connectivity between the medial frontal cortex and the fusiform in the low gamma more for social stimuli than for non-social ones, a reduction that was correlated with individuals’ performance in the task. Additionally, for both social and non-social stimuli, OT increased the connectivity in the alpha and beta bands. Limitations Sample size was determined based on sample sizes previously reported in MEG in clinical populations, especially OT administration studies in combination with neuroimaging in ASD. We were limited in our capability to recruit for such a study, and as such, the sample size was not based on a priori power analysis. Additionally, we limited our analyses to specific neural bands and regions. To validate the current results, future studies may be needed to explore other parameters using whole-brain approaches in larger samples. Conclusion These results suggest that OT influenced social perception by modifying the communication between frontal and posterior regions, an attenuation that potentially impacts both social and non-social early perception. We also show that OT influences differ between top-down and bottom-up processes, depending on the social context. Overall, by showing that OT influences both social-related perception and overall attention during early processing stages, we add new information to the existing understanding of the impact of OT on neural processing in ASD. Furthermore, by highlighting the influence of OT on early perception, we provide new directions for treatments for difficulties in early attentional phases in this population. Trial registration Registered on October 27, 2021—Retrospectively registered, https://clinicaltrials.gov/ct2/show/record/NCT05096676 (details on clinical registration can be found in www.clinicalTrial.gov, unique identifier: NCT05096676).

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Children with autism spectrum disorder show altered functional connectivity and abnormal maturation trajectories in response to inverted faces

Cited by 14 publications

References 85 publications

Functional Significance of Human Resting-State Networks Hubs Identified Using MEG During the Transition From Childhood to Adulthood

Functional Significance of Human Resting-State Networks Hubs Identified Using MEG During the Transition From Childhood to Adulthood

The Directionality of Fronto-Posterior Brain Connectivity Is Associated with the Degree of Individual Autistic Traits

Oxytocin impacts top-down and bottom-up social perception in adolescents with ASD: a MEG study of neural connectivity

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