Shared and idiosyncratic cortical activation patterns in autism revealed under continuous real‐life viewing conditions

Abstract

Scientific abstract Although widespread alterations in cortical structure have been documented in individuals with autism, the functional implications of these alterations remain to be determined. Here, we adopted a novel inter-subject (inter-SC) and intra-subject (intra-SC) correlation technique to quantify the reliability of the spatio-temporal responses of functional MR activity across the entire cortex in adults with autism during free-viewing of a popular audio-visual movie. Whereas these complex stimuli evoke highly reliable shared response time courses in typical individuals, cortical activity was more variable across individuals with autism (low inter-SC). Interestingly, when we measured the responses within an autistic individual across repeated presentations of the movie, we observed a unique, idiosyncratic response time course that was reliably replicated within each individual (high intra-SC). Encouragingly, after filtering out the idiosyncratic responses from each individual time course, we were able to uncover a more typical response profile, which resembles the shared responses seen in the typical subjects. These findings indicate that, under conditions approximating real-life situations, the neural activity of individuals with autism is characterized by individualistic responses that, although reliable within an autistic individual, are both highly variable across autistic individuals and different from the responses observed within the typical subjects. These idiosyncratic responses may underlie the atypical behaviors observed in autism. At the same time, we are encouraged by the presence of the more typical activation pattern lurking beneath these idiosyncratic fluctuations. Taken together, these findings may pave the way to future research aimed at characterizing the idiosyncratic response profiles, which, in turn, might contribute to a better understanding of the heterogeneity of the autism spectrum and its diagnosis.

Brain dynamics in ASD during movie‐watching show idiosyncratic functional integration and segregation

“…However, they show that the idiosyncrasy in brain responses previously reported across ASD subjects in stationary computational settings (Hasson et al, 2009; Hahamy, Behrmann, & Malach, 2015; Salmi et al, 2013) concerns precisely timed movie events involving functional integration and segregation.…”

“…By correlating a given regional time course of activity across subjects, a measure of response homogeneity can be obtained. This approach revealed globally more idiosyncratic activity in ASD than in typically developing (TD) individuals (Hasson et al, 2009; Salmi et al, 2013). However, as a movie involves a continuously changing sequence of temporally overlapping cues, to which the brain dynamically adjusts, such stationary analyses (i.e., through one estimate for the whole task duration) may fall short of an accurate characterization.…”

Autism Spectrum Disorder: Does Neuroimaging Support the DSM-5 Proposal for a Symptom Dyad? A Systematic Review of Functional Magnetic Resonance Imaging and Diffusion Tensor Imaging Studies

“…Secondly, results of task-related studies could be biased by the confounding effect of abnormal visual fixation patterns commonly present in patients with ASD and of their lower degree of success, motivation, and interest when performing these tasks (Hadjikhani et al 2006;Klin 2008;Yerys et al 2009). Thirdly, studies usually point to the presence of highly variable individualistic responses in different patients with ASD (Hasson et al 2009), and tend not to differentiate between subgroups, such as patients with autism (low-and high-functioning) or patients with Asperger syndrome. Only a small number of studies have been conducted in patients with Asperger syndrome (Bloemen et al 2010;Catani et al 2008;Nishitani et al 2004;Oktem et al 2001;Pugliese et al 2009;Shamay-Tsoory et al 2010), and none of them have directly compared processing abnormalities between patients with high-functioning autism and patients with Asperger syndrome, which may be interesting for refining the neuroanatomical substrate of their language and social deficits.…”

Neural variability: friend or foe?

“…The relationship between neural variability and functional or structural connectivity throughout development has not been examined thus far. An additional hypothesis is that individuals with autism develop altered perceptual systems that exhibit heightened sensitivity to details [54] together with an impaired ability to integrate details coherently into gestalt percepts [55] such as faces [56]. Whereas a heightened sensitivity to details seems to be at odds with the idea of excessive neural variability, it has been proposed that the greater presence of neural noise in autism may have a counterintuitive beneficial effect of enhancing detection of details as a result of stochastic resonance [24].…”