A Neuroanatomical Substrate Linking Perceptual Stability to Cognitive Rigidity in Autism

Abstract

Overly stable visual perception seen in individuals with autism spectrum disorder (ASD) is related to higher-order core symptoms of the condition. However, the neural basis by which these seemingly different symptoms are simultaneously observed in individuals with ASD remains unclear. Here, we aimed to identify such a neuroanatomical substrate linking perceptual stability to autistic cognitive rigidity, a part of core restricted, repetitive behaviors (RRBs). First, using a bistable visual perception test, we measured the perceptual stability of 22 high-functioning adults with ASD and 22 age-, IQ-, and sex-matched typically developing human individuals and confirmed overstable visual perception in autism. Next, using a spontaneous task-switching (TS) test, we showed that the individuals with ASD were more likely to repeat the same task voluntarily and spontaneously, and such rigid TS behavior was associated with the severity of their RRB symptoms. We then compared these perceptual and cognitive behaviors and found a significant correlation between them for individuals with ASD. Finally, we found that this behavioral link was supported by a smaller gray matter volume (GMV) of the posterior superior parietal lobule (pSPL) in individuals with ASD. Moreover, this smaller GMV in the pSPL was also associated with the RRB symptoms and replicated in two independent datasets. Our findings suggest that the pSPL could be one of the neuroanatomical mediators of cognitive and perceptual inflexibility in autism, which could help a unified biological understanding of the mechanisms underpinning diverse symptoms of this developmental disorder. SIGNIFICANCE STATEMENT Behavioral studies show perceptual overstability in autism spectrum disorder (ASD). However, the neural mechanisms by which such sensory symptoms can coexist and often correlate with seemingly separate core symptoms remain unknown. Here, we have identified such a key neuroanatomical substrate. We have revealed that overstable sensory perception of individuals with ASD is linked with their cognitive rigidity, a part of core restricted, repetitive behavior symptoms, and such a behavioral link is underpinned by a smaller gray matter volume in the posterior superior parietal lobule in autism. These findings uncover a key neuroanatomical mediator of autistic perceptual and cognitive inflexibility and would ignite future studies on how the core symptoms of ASD interact with its unique sensory perception.

Atypical Facial Emotion Recognition in Children with Autism Spectrum Disorders: Exploratory Analysis on the Role of Task Demands

“…Neuroimaging studies, using functional magnetic resonance imaging (fMRI), however, have shown atypical activation in the amygdala and fusiform gyrus in ASD during FER (Ashwin et al, 2007;Critchley et al, 2000). There is growing evidence for an atypical functionality in the posterior cingulate cortex and ventromedial prefrontal cortex in ASD (Lau et al, 2020), and the disruption of their connectivity is related to a cognitive inflexibility, a central feature of ASD (Watanabe et al, 2019). The posterior cingulate cortex also mediates between visual and emotional processing (Vogt et al, 2006) and its disruption results in difficulties in children with ASD in socio-emotional processes.…”

Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics

“…6b). Considering that the perceptual stability seen in this bistable perception test was relevant to autistic cognitive rigidity 46 , these longitudinal observations may become a basis for new clinical noninvasive neural interventions and accelerate the development of such state-dependent brain stimulation methods. Fig.…”

“…The test design of bistable visual perception paradigm in this study is essentially the same as that used in our previous work 19,46 . The participants were presented with a structure-from-motion (SFM) stimulus (Fig.…”

Right Temporoparietal Junction Underlies Avoidance of Moral Transgression in Autism Spectrum Disorder

“…Another possible explanatory factor of ASD participants' tendency to make overly-moral decisions in the Bad context is behavioral rigidity, a core symptom for clinical diagnosis of ASD (APA, 2013). Previous studies have revealed that compared with healthy controls, individuals with ASD were more likely to show repetitive behaviors in a variety of cognitive tasks (D'Cruz et al, 2013;Watanabe et al, 2019). Hence, it is possible that behavioral rigidity, at least to some extent, is a more general mechanism that contributes to the overly-moral behaviors in the Bad context (i.e., rejecting over 85% of the trials).…”