Neural Mechanisms of Facial Emotion Recognition in Autism: Distinct Roles for Anterior Cingulate and dlPFC

ABSTRACT

Objective

The present study sought to measure and internally validate neural markers of facial emotion recognition (FER) in adolescents and young adults with ASD to inform targeted intervention.

Method

We utilized fMRI to measure patterns of brain activity among individuals with ASD (N = 21) and matched controls (CON; N = 20) 2 s prior to judgments about the identity of six distinct facial emotions (happy, sad, angry, surprised, fearful, disgust).

Results

Predictive modeling of fMRI data (support vector classification; SVC) identified mechanistic roles for brain regions that forecasted correct and incorrect identification of facial emotion as well as sources of errors over these decisions. BOLD signal activation in bilateral insula, anterior cingulate (ACC) and right dorsolateral prefrontal cortex (dlPFC) preceded accurate FER in both controls and ASD. Predictive modeling utilizing SVC confirmed the utility of ACC in forecasting correct decisions in controls but not ASD, and further indicated that a region within the right dlPFC was the source of a type 1 error signal in ASD (i.e. neural marker reflecting an impending correct judgment followed by an incorrect behavioral response) approximately two seconds prior to emotion judgments during fMRI.

Conclusions

ACC forecasted correct decisions only among control participants. Right dlPFC was the source of a false-positive signal immediately prior to an error about the nature of a facial emotion in adolescents and young adults with ASD, potentially consistent with prior work indicating that dlPFC may play a role in attention to and regulation of emotional experience.

Disclosure Statement

All authors of this study report no conflict of interest, financial or otherwise.

Notes

¹ We opted to include only men in this study, based on the following factors: (1) prior work indicating that ASD is predominantly diagnosed in men, (2) evidence that FER abilities may vary by sex, and (3) due to the small sample size sought here.

² We further probed the possibility that certain individuals may have been differentially motivated to respond faster to each event because of the implicit relationship between faster responses and the total duration of the run. In other words, it is conceivable that some individuals may have been motivated to respond faster specifically because briefer trials would collectively result in a briefer overall experimental session for that participant. However, we found no correlations between trial number and reaction time or error rate at the group level nor did we observe outliers when evaluating cases individually. We further found no evidence that any participant’s performance approached chance levels in the forced choice phase of the task, thus supporting the notion that participants in general complied with the instructions as given.

³ The decision to conclude the morph and transition to a fixation cross was made to avoid the possibility that continuing the morphing sequence could contradict prior belief in the facial emotion identity and therefore introduce noise from other potential psychological processes such as error monitoring and subsequent learning effects. This would have been disproportionately detrimental to isolating BOLD variance on error trials more so than correct trials, and so we designed that task so that a button press would immediately terminate the stimulus and initiate a blank screen with a fixation cross.

⁴ Stability is defined as the amount of change in the output of the decoder as a function of small changes in the data on which the decoder is trained (Shalev-Shwartz et al., 2010).

Additional information

Funding

This work was supported by the National Institutes of Health, National Institute of Mental Health (NIH/NIMH) under grant number MH100268.