Animal, but not human, faces engage the distributed face network in adolescents with autism

Abstract

Multiple hypotheses have been offered to explain the impaired face-processing behavior and the accompanying underlying disruptions in neural circuitry among individuals with autism. We explored the specificity of atypical face-processing activation and potential alterations to fusiform gyrus (FG) morphology as potential underlying mechanisms. Adolescents with high functioning autism (HFA) and age-matched typically developing (TD) adolescents were scanned with sMRI and fMRI as they observed human and animal faces. In spite of exhibiting comparable face recognition behavior, the HFA adolescents evinced hypo-activation throughout the face-processing system in response to unfamiliar human, but not animal, faces. They also exhibited greater activation in affective regions of the face-processing network in response to animal, but not human, faces. Importantly, this atypical pattern of activation in response to human faces was not related to atypical structural properties of the FG. This atypical neural response to human faces in autism may stem from abnormalities in the ability to represent the reward value of social (i.e. conspecific) stimuli.

Efficient human face detection in infancy

“…Finally, infants' face attentional efficiency-detection, attention capture, and attention holding-may hold promise for identifying early abnormalities which may indicate heightened risk for disorders (e.g., autism: Elsabbagh et al, 2013aElsabbagh et al, , 2013bSchultz, 2005; prosopagnosia: Dalrymple & Duchaine, 2015). While neurotypical populations find human faces more rewarding than animal faces, autistic populations exhibit the reverse (Whyte et al, 2015). Assessing the development of OSB in these populations may prove insightful.…”

“…However, studies thus far cannot determine whether these biases are due to general face properties (e.g., first-order relations of facial elements) or are exclusive to human faces, as face detection for human and animal faces has not been compared. In adults, animal faces engage similar visual processing as human faces (Diamond & Carey, 1986) and elicit similar neural activation (Blonder et al, 2004); therefore, comparisons of human and animal face processing can disentangle developmental patterns in face processing generally from human face processing specifically (Whyte, Behrmann, Minshew, Garcia, & Scherf, 2015). While adults exhibit an OSB in face detection (Simpson, Buchin, Werner, Worrell, & Jakobsen, 2014a), it is unclear when this bias emerges.…”

A theoretical rut: revisiting and critically evaluating the generalized under/over‐connectivity hypothesis of autism

“…For example, we have recently written about the likelihood that adolescence is a developmental period of vulnerability in autism (Picci & Scherf, 2015), which is supported by both behavioral and neuroimaging findings (e.g. Scherf, Behrmann, Kimchi & Luna, 2009;Scherf, Luna, Minshew & Behrmann, 2010;Scherf et al, 2015;Whyte et al, 2016). Taking a developmental perspective with this in mind could lead to hypotheses about how neural networks are changing in adolescence.…”

“…This region of interest (ROI) approach has led to core findings about atypical activation in numerous regions, particularly those that are implicated in processing socially relevant stimuli such as faces and their concurrent emotions (e.g. Scherf, Elbich, Minshew & Behrmann, 2015;Weng, Carrasco, Swartz, Wiggins, Kurapati et al, 2011;Whyte, Behrmann, Minshew, Garcia & Scherf, 2016). Approximately 15 years ago, researchers began to evaluate whether there are atypicalities in the functional interactions between brain regions in autism.…”

Face Detection and the Development of Own‐Species Bias in Infant Macaques

“…Our goal was to clarify the development of face processing generally from conspecific face processing (Whyte, Behrmann, Minshew, Garcia, & Scherf, ). We hypothesized that 3‐week‐olds, despite little face experience, would prioritize attention to face stimuli, reflected behaviorally in face biases (Frank, Amso, & Johnson, ; Macchi Cassia, Simion, & Umiltà, ).…”