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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Available from: A Ting Wang, Aug 20, 2015
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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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    ABSTRACT: Previous studies have shown that brain regions for mentalizing, including temporoparietal junction (TPJ) and medial prefrontal cortex (mPFC), are activated in understanding the nonliteral meaning of sentences. A different set of brain regions, including left inferior frontal gyrus (IFG), is activated for dealing with pragmatic incongruence. Here we demonstrate that individuals’ cognitive empathic ability modulates the brain activity underlying the processing of pragmatic constraints during sentence comprehension. The lian … dou … construction in Chinese (similar to English even) normally describes an event of low expectedness; it also introduces a pragmatic scale against which the likelihood of an underspecified event can be inferred. By embedding neutral or highly likely events in the construction, we created underspecified and incongruent sentences and compared both with control sentences in which events of low expectedness were described. Imaging results showed that (i) left TPJ was activated for the underspecified sentences, and the activity in mPFC correlated with individuals’ fantasizing ability and (ii) anterior cingulate cortex (ACC) was activated for the incongruent sentences, and the activity in bilateral IFG correlated with individuals’ perspective taking ability. These findings suggest that brain activations in making pragmatic inference and in dealing with pragmatic failure are modulated by different components of cognitive empathy.
    Social Cognitive and Affective Neuroscience 08/2014; 9(8):1166-1174. DOI:10.1093/scan/nst091 · 5.88 Impact Factor
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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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    ABSTRACT: The frontal lobes are involved in many higher-order cognitive functions such as social cognition executive functions and language and speech. These functions are complex and follow a prolonged developmental course from childhood through to early adulthood. Magnetoencephalography (MEG) is ideal for the study of development of these functions, due to its combination of temporal and spatial resolution which allows the determination of age-related changes in both neural timing and location. There are several challenges for MEG developmental studies: to design tasks appropriate to capture the neurodevelopmental trajectory of these cognitive functions, and to develop appropriate analysis strategies to capture various aspects of neuromagnetic frontal lobe activity. Here, we review our MEG research on social and executive functions, and speech in typically developing children and in two clinical groups - children with autism spectrum disorder and children born very preterm. The studies include facial emotional processing, inhibition, visual short-term memory, speech production, and resting-state networks. We present data from event-related analyses as well as on oscillations and connectivity analyses and review their contributions to understanding frontal lobe cognitive development. We also discuss the challenges of testing young children in the MEG and the development of age-appropriate technologies and paradigms.
    Frontiers in Human Neuroscience 06/2014; 8:453. DOI:10.3389/fnhum.2014.00453 · 2.90 Impact Factor
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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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    ABSTRACT: Individuals with autism spectrum disorders (ASD) have difficulty understanding other minds (Theory of Mind; ToM), with atypical processing evident at both behavioural and neural levels. Individuals with conduct problems and high levels of callous-unemotional (CU) traits (CP/HCU) exhibit reduced responsiveness to others' emotions and difficulties interacting with others, but nonetheless perform normally in experimental tests of ToM. The present study aimed to examine the neural underpinnings of ToM in children (aged 10–16) with ASD (N = 16), CP/HCU (N = 16) and typically developing (TD) controls (N = 16) using a non-verbal cartoon vignette task. Whilst individuals with ASD were predicted to show reduced fMRI responses across regions involved in ToM processing, CP/HCU individuals were predicted to show no differences compared with TD controls. The analyses indicated that neural responses did not differ between TD and CP/HCU groups during ToM. TD and CP/HCU children exhibited significantly greater medial prefrontal cortex responses during ToM than did the ASD group. Within the ASD group, responses in medial prefrontal cortex and right temporoparietal junction (TPJ) correlated with symptom severity as measured by the Autism Diagnostic Observation Schedule (ADOS). Findings suggest that although both ASD and CP/HCU are characterized by social difficulties, only children with ASD display atypical neural processing associated with ToM.
    Developmental Science 03/2014; 17(5). DOI:10.1111/desc.12167 · 3.89 Impact Factor
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