Neural responses to emotional expression information in high- and low-spatial frequency in autism: evidence for a cortical dysfunction

Abstract

Despite an overall consensus that Autism Spectrum Disorder (ASD) entails atypical processing of human faces and emotional expressions, the role of neural structures involved in early facial processing remains unresolved. An influential model for the neurotypical brain suggests that face processing in the fusiform gyrus and the amygdala is based on both high-spatial frequency (HSF) information carried by a parvocellular pathway, and low-spatial frequency (LSF) information separately conveyed by a magnocellular pathway. Here, we tested the fusiform gyrus and amygdala sensitivity to emotional face information conveyed by these distinct pathways in ASD individuals (and matched Controls). During functional Magnetical Resonance Imaging (fMRI), participants reported the apparent gender of hybrid face stimuli, made by merging two different faces (one in LSF and the other in HSF), out of which one displayed an emotional expression (fearful or happy) and the other was neutral. Controls exhibited increased fusiform activity to hybrid faces with an emotional expression (relative to hybrids composed only with neutral faces), regardless of whether this was conveyed by LSFs or HSFs in hybrid stimuli. ASD individuals showed intact fusiform response to LSF, but not HSF, expressions. Furthermore, the amygdala (and the ventral occipital cortex) was more sensitive to HSF than LSF expressions in Controls, but exhibited an opposite preference in ASD. Our data suggest spared LSF face processing in ASD, while cortical analysis of HSF expression cues appears affected. These findings converge with recent accounts suggesting that ASD might be characterized by a difficulty in integrating multiple local information and cause global processing troubles unexplained by losses in low spatial frequency inputs.

Differences in cortical processing of facial emotions in broader autism phenotype

“…Thereby, our results might be evidence that the perception of emotional facial expressions depends on a neural network that entails the perception of changeable features of the human face that are crucial for social communication (Deen & Saxe, 2019;Andrews & Ewbank, 2004). The decrease in the modulation of the temporal brain region observed in pASD ( Figure 5, bottom line, left row) might reveal that differences between ASD and neurotypical development in cortical processing of faces expressing emotion could be broader and more complex than a mere consequence of social difficulties, and should receive more attention in future research (Billeci et al, 2016;Gerdts and Bernier, 2011;Sucksmith et al, 2011, Spencer et al, 2011Corradi-Dell'Acqua et al, 2014;Jackson et al, 2013). Indeed, the activation of this brain area correlates negatively with the symptomatology of their children (in terms of ADOS-2 score).…”

“…Several studies have reported that ASD affects face perception (Luyster et al, 2014;Chawarska, Ye, Shic, & Chen, 2016;Jones & Klin, 2013). These impairments seem to depend on the spatial frequency of the visual stimuli (McCleery et al, 2007;Jackson et al, 2013;Corradi-Dell'Acqua et al, 2014). The perception of different spatial frequencies of visual stimuli relies on two types of retinal neurons that process either fine or coarse resolution of the visual signal (Vuilleumier et al, 2003;Boutet et al, 2003).…”

“…On one hand, the magnocellular (M) visual pathway, involves the ganglion cells of the retina with a large receptive field and participates in the perception of low resolution imaging without details (low-spatial frequency). On the other hand, the parvocellular (P) visual pathway is comprised by retinal ganglion cells with small receptive fields and serves to discriminate fine details of a scene and the color (high-spatial frequency) (Kandel et al, 2000;McCleery et al, 2007;Jackson et al, 2013;Corradi-Dell'Acqua et al, 2014). Evidence shows that face perception depends on high-spatial frequencies (HSF) that provides crucial information for a precise recognition and identification in the ventral extrastriate cortex (Vuilleumier et al, 2003;Boutet et al, 2003).…”

“…Certainly, this evidence might suggest that alterations in face processing in ASD are more related with a difficulty in integrating multiple local sources of information rather than alterations in one pathway only. Moreover, the notion that detailed information of the facial stimuli is processed only by HSF and global configurations can be processed only by LSF seems quite confusing (Corradi-Dell'Acqua et al, 2014). Indeed, studies have revealed that face perception crucially requires the integration of both visual pathways (Pessoa et al, 2010;Corradi-Dell'Acqua et al, 2014;Boutet et al, 2003).…”

Shortcuts for fear in hierarchical visual systems

“…Therefore, spatial frequency filtering may not be an effective way of isolating subcortical input to the amygdala via the pulvinar (although it remains to be seen whether it still may be viable for isolating input from the superior colliculus, specifically). This is a critical contribution to the current literature on emotion processing, which has already made inferences about autism by using spatial frequency as a proxy for subcortical processing (Corradi-Dell'Acqua et al, 2014).…”