Article

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

Department of Psychiatry, University of California, Los Angeles, USA.
Archives of General Psychiatry (Impact Factor: 13.75). 07/2007; 64(6):698-708. DOI: 10.1001/archpsyc.64.6.698
Source: PubMed

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

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    • "For example, a conversational utterance or a statement that demands an inferential process to arrive at its nonliteral interpretation , such as an ironic remark (Shibata et al., 2010; Bohrn et al., 2012; Spotorno et al., 2012) or an indirect request (Van Ackeren et al., 2012), may engender activation of brain regions typically involved in mentalizing or cognitive empathy (Saxe and Kanwisher, 2003; Saxe, 2006; see Van Overwalle, 2009; Van Overwalle and Baetens, 2009 for meta-analysis ), including temporoparietal junction area (TPJ) and medial prefrontal cortex (mPFC). Patients with autism spectrum disorders, who show deficits in their ability to infer the pragmatic meaning of metaphors (Sperber and Wilson, 1987; Happe, 1993) or ironic remarks (Happe, 1993; Martin and McDonald, 2004), have reduced brain activity in the mPFC and TPJ (Wang et al., 2007). "
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    • "Behavioral studies have consistently reported difficulties with face processing in children with ASD, and this population has also been shown to exhibit poor eye contact (Hobson and Lee, 1998) as well as a reduced tendency to look at the faces of others (Langdell, 1978). Prior work investigating neural responses to emotional faces in ASD have demonstrated activation of brain regions implicated in social cognition, including medial prefrontal and STS regions (Pierce et al., 2001; Pelphrey et al., 2007; Wang et al., 2007). ERP studies have also demonstrated that early responses to emotional faces in children with ASD were delayed and smaller (Wong et al., 2008; Batty et al., 2011). "
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    • "One study, using static cartoon stimuli in children aged 7 to 16 with and without ASD, reported significantly reduced activation in mPFC, STS, left temporal pole, and precuneus during ToM (Carter et al., 2012). The two other studies have reported similar results, including negative correlations between autistic social symptoms and superior temporal responses (Wang et al., 2006), and between social responsiveness and medial PFC activation (Wang, Lee, Sigman & Dapretto, 2007). "
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