Atypical Medial Prefrontal Cortex Response to Implicit Emotion Processing in Autism Spectrum Disorders

Background:  Inferring others’ emotions and intentions is critical in successful social interaction.  Many individuals with autism spectrum disorders (ASD) struggle in navigating the social world, largely due to difficulty reading others’ emotions from faces (Harms et al., 2010) and from body postures (Hadjikhani et al., 2009). Nevertheless, such difficulty may be less pronounced when the emotion is explicit and more pronounced when the emotion is implicit. This difference and its neural bases have been relatively under-examined in ASD. The fMRI study reported here uses dynamic action scenarios to examine the neural mechanisms underlying explicit and implicit emotion processing in ASD.

Objectives:  The purpose of this fMRI study was to examine the brain activation and functional connectivity differences associated with implicit emotion processing in individuals with ASD and typically developing (TD) control participants.

Methods:  17 high-functioning adults with ASD (mean age = 24.5) and 15 TD adults (mean age = 24.7) watched a series of short videos (average length = 10 seconds) in a Siemens 3T MRI scanner. The videos, presented in an event-related design, consisted of an action or social interaction involving either one actor or two actors (emotions: happy, sad, angry, and afraid). Participants were asked to either determine the emotional state of an individual (explicit emotion processing) or to identify a specific object in the video (implicit emotion processing). There was also a control condition, where participants watched neutral videos and were asked to make a perceptual judgment. The fMRI data were analyzed using SPM8 (Statistical Parametric Mapping) software. 

Results: Statistically significant group differences in brain activity were seen only during implicit emotion processing, with participants with ASD showing reduced activity, relative to TD participants, in medial prefrontal cortex (MPFC) and bilateral superior temporal sulcus (p=0.001; cluster size =72mm³). Functional connectivity analysis revealed significantly weaker connectivity between several networks in the ASD participants during implicit emotional processing, especially the connections between MPFC and other regions like amygdala, STS, IPL, and fusiform gyrus. Behavioral analyses revealed that the ASD participants performed explicit emotion processing equally well as the TD control participants. However, the ASD participants made significantly more errors, compared to TD controls (ASD mean=70%; TD mean=91%), making non-emotion judgments during implicit emotion processing [t(30)=2.3; p < 0.05].

Conclusions:  The findings of this study underscore the importance of MPFC in emotion processing. Decreased activation and connectivity of the MPFC, along with decreased performance in non-emotion judgment during implicit emotion processing in the ASD group suggest impairments in autism in the neural circuitry underlying automatic processing of emotions. The MPFC is a crucial brain region for implicit emotional processing; the connectivity of MPFC with amygdala has been found to be critical in emotion regulation (Zink et al., 2010).