Reading affect in the face and voice: neural correlates of interpreting communicative intent in children and adolescents with autism spectrum disorders

Abstract

Context: Understanding a speaker's communicative intent in everyday interactions is likely to draw on cues such as facial expression and tone of voice. Prior research has shown that individuals with autism spectrum disorders (ASD) show reduced activity in brain regions that respond selectively to the face and voice. However, there is also evidence that activity in key regions can be increased if task demands allow for explicit processing of emotion.

Objectives: To examine the neural circuitry underlying impairments in interpreting communicative intentions in ASD using irony comprehension as a test case, and to determine whether explicit instructions to attend to facial expression and tone of voice will elicit more normative patterns of brain activity.

Design, setting, and participants: Eighteen boys with ASD (aged 7-17 years, full-scale IQ >70) and 18 typically developing (TD) boys underwent functional magnetic resonance imaging at the Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles.

Main outcome measures: Blood oxygenation level-dependent brain activity during the presentation of short scenarios involving irony. Behavioral performance (accuracy and response time) was also recorded.

Results: Reduced activity in the medial prefrontal cortex and right superior temporal gyrus was observed in children with ASD relative to TD children during the perception of potentially ironic vs control scenarios. Importantly, a significant group x condition interaction in the medial prefrontal cortex showed that activity was modulated by explicit instructions to attend to facial expression and tone of voice only in the ASD group. Finally, medial prefrontal cortex activity was inversely related to symptom severity in children with ASD such that children with greater social impairment showed less activity in this region.

Conclusions: Explicit instructions to attend to facial expression and tone of voice can elicit increased activity in the medial prefrontal cortex, part of a network important for understanding the intentions of others, in children with ASD. These findings suggest a strategy for future intervention research.

Figure 1

Example scenario. The setup (top) is shared by both the sincere and ironic versions of the scenario. The sincere ending is shown at the bottom left, and the ironic ending is displayed at the bottom right. The text below the drawings represents the accompanying auditory stimuli. Participants view the setup first, then either the sincere or ironic version of a scenario, followed by a blank screen and the question, “Did Ed mean what he said?”

Figure 2

Brain activity during potentially ironic scenarios relative to rest. A, Significant activity was observed in the medial prefrontal cortex and the left inferior frontal gyrus in the typically developing (TD) group but not the autism spectrum disorders (ASD) group when instructions were neutral. B, Both groups engaged prefrontal regions when explicit instructions were provided to attend to the facial expression or tone of voice of the speaker. Activation exceeds thresholds of P<.05 corrected for multiple comparisons at the cluster level (k≥115) and P<.05 at the voxel level (t>2.57 at peaks). Yellow arrowheads indicate medial prefrontal cortex; green arrowheads, left inferior frontal gyrus.

Figure 3

Activity in the medial prefrontal cortex as a function of symptom severity. A negative correlation was found in children with autism spectrum disorders between activity in the medial prefrontal cortex and scores on the Social Responsiveness Scale (higher scores indicate greater social impairment). Activation exceeds thresholds of P<.05 corrected for multiple comparisons at the cluster level (k≥115) and P<.05 at the voxel level (t>2.57 at peaks).