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: 14.48). 07/2007; 64(6):698-708. DOI: 10.1001/archpsyc.64.6.698
Source: PubMed


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.

Download full-text


Available from: A Ting Wang
  • Source
    • "The majority of neuroimaging research investigating ToM in ASD suggests reduced blood oxygen level dependent (BOLD) activity within these frontal (e.g.Castelli et al. 2002; Lombardo et al. 2011; Wang et al. 2007) and temporoparietal [bilateral superior temporal gyrus and, left middle temporal gyrus (Wang et al. 2007); bilateral TPj and the posterior cingulate cortex/precuneus (Lombardo et al. 2011); temporal poles, and the superior temporal sulcus (STS) at the TPj (Castelli et al. 2002)] regions in adolescents and adults with high-functioning ASD compared to NT controls. This is often described as a negative relationship between social impairment and BOLD activity (Castelli et al. 2002; Lombardo et al. 2011; Silani et al. 2008; Wang et al. 2007). In contrast to the majority of the literature however, White et al. (2014) note increased mentalizing network activity in individuals with ASD compared to controls. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The medial prefrontal cortex (mPFC) and the right temporo-parietal junction (rTPj) are highly involved in social understanding, a core area of impairment in autism spectrum disorder (ASD). We used fMRI to investigate sex differences in the neural correlates of social understanding in 27 high-functioning adults with ASD and 23 matched controls. There were no differences in neural activity in the mPFC or rTPj between groups during social processing. Whole brain analysis revealed decreased activity in the posterior superior temporal sulcus in males with ASD compared to control males while processing social information. This pattern was not observed in the female sub-sample. The current study indicates that sex mediates the neurobiology of ASD, particularly with respect to processing social information.
    Full-text · Article · Nov 2015 · Journal of Autism and Developmental Disorders
    • "All of these network components have been previously identified as clinical hallmarks in ASD. For example, functional differences in parahippocampal, fusiform and lingual cortices have previously been linked to impairments in face and visuospatial processing (Kleinhans et al., 2008; McGrath et al., 2012); the precuneus has a role in emotion, self-referential thinking and projection processes critical for social development (Cavanna and Trimble, 2006) and has also been linked to atypical mentalizing or theory of mind in ASD (Castelli et al., 2002; Wang et al., 2007); the paracentral and superior parietal cortices are part of the network alleged to be the basis of imitative and empathic behavior (Rizzolatti and Craighero, 2004), and have also been proposed to underpin ASD deficits in motor control, Table 2 Integrity and connectivity-closeness values of the brain regions used to derive group structural covariance networks for ASD and control subjects. Significant differences (FDR corrected) between groups were observed only for the integrity-closeness measure. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Autism spectrum disorders (ASD) are a group of neurodevelopmental conditions characterized by atypical structural and functional brain connectivity. Complex network analysis has been mainly used to describe altered network-level organization for functional systems and white matter tracts in ASD. However, atypical functional and structural connectivity are likely to be also linked to abnormal development of the correlated structure of cortical gray matter. Such covariations of gray matter are particularly well suited to the investigation of the complex cortical pathology of ASD, which is not confined to isolated brain regions but instead acts at the systems level. In this study, we examined network centrality properties of gray matter networks in adults with ASD (n = 84) and neurotypical controls (n = 84) using graph theoretical analysis. We derived a structural covariance network for each group using interregional correlation matrices of cortical volumes extracted from a surface-based parcellation scheme containing 68 cortical regions. Differences between groups in closeness network centrality measures were evaluated using permutation testing. We identified several brain regions in the medial frontal, parietal and temporo-occipital cortices with reductions in closeness centrality in ASD compared to controls. We also found an association between an increased number of autistic traits and reduced centrality of visual nodes in neurotypicals. Our study shows that ASD are accompanied by atypical organization of structural covariance networks by means of a decreased centrality of regions relevant for social and sensorimotor processing. These findings provide further evidence for the altered network-level connectivity model of ASD.
    No preview · Article · Sep 2015 · Journal of Psychiatric Research
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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.
    Full-text · Article · Aug 2014 · Social Cognitive and Affective Neuroscience
Show more