PMC:4300004 / 28757-39960 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/4300004","sourcedb":"PMC","sourceid":"4300004","source_url":"http://www.ncbi.nlm.nih.gov/pmc/4300004","text":"4.2 Neuroimaging\nOur MEG findings demonstrate a complex progression of both over- and under-activation in the frontal, temporal, tempo-parietal, and limbic brain regions. Of particular interest was the abnormal neural activity in areas of the ‘social brain’, which encompass the ACC and orbitofrontal cortex (Brothers, 2002). The network of neural areas showing atypical activation is consistent with the model of anomalous long-range projections and the subsequent recruitment of greater processing networks in ASD (Courchesne \u0026 Pierce, 2005; Just et al., 2004). While typically developing individuals successfully integrate and coordinate multiple cognitive domains within a network of neural structures, our data suggest that individuals with ASD have deficits in the recruitment of comparable brain regions, including the orbitofrontal, limbic, and temporal regions, which impact their abilities with facial affect processing.\n\n4.2.1 Atypical cingulate activation: delayed functional specialization of threat-relevant affective processing in ASD\nAdolescents with ASD showed reduced left ACC and late right posterior cingulate (PCC) activation to angry faces and early right ACC and PCC underactivation to happy faces. The cingulate gyrus is functionally and cytoarchitecturally heterogeneous, with the anterior and posterior regions reciprocally connected with different regions of the brain (see Vogt et al., 1992 for a review). Classically, the cingulate gyrus is divided into the ACC and PCC, with the former linked to executive functioning, including affective processing, and the latter associated with evaluative processes (Vogt et al., 1992).\nIn ASD structural, functional and cyto-architectural idiosyncrasies of the ACC have been reported (e.g., Haznedar et al., 1997; Simms et al., 2009). In typically developing children, a shift from only the amygdala to the amygdala and ACC activity during threat-relevant affect processing has been shown, with children utilizing the earlier-developing subcortical structures involving the amygdala and adolescents employing the later maturing functionally specialized cortical route that includes the ACC (Hung et al., 2012). Our data showing consistently reduced ACC activation in ASD is congruent with the notion of immature processing of angry faces in adolescents with ASD, relative to their typically developing peers.\nInterestingly, decreased right PCC activation in ASD was noted only to happy faces. As a canonical ‘evaluative’ region, the PCC is implicated in monitoring and assessing the external environment (Vogt et al., 1992). In typically developing children increased PCC activity to both happy and fearful faces relative to a non-emotional cognitive task has been noted (Habel et al., 2005). Reduced activation in the PCC in adolescents with ASD suggests its inadequate recruitment and, is in line with overall limbic underactivation in ASD.\n\n4.2.2 Orbitofrontal underactivation in ASD to angry faces\nAdolescents with ASD showed less orbitofrontal activity first in the left orbitofrontal area and then bilaterally compared to controls in response to angry faces. Closely connected to the amygdala, insula and ACC, the orbitofrontal cortex has been implicated in social inhibition and behaviour mediation (Blair et al., 1999; Dias et al., 1996; Elliott et al., 2000; Rolls, 2004; Van Honk et al., 2005). Insensitivity to both punishment and reward and emotion dysregulation has been observed following orbitofrontal damage (Berlin et al., 2004). Furthermore, the orbitofrontal cortex has been implicated in associating stimuli with behavioural outcome, which is integral for outcome predictions for adaptive behaviour (see Rushworth et al., 2007 for a review) as well as inferring others' emotional states (Baron-Cohen et al., 1999). Impairments in representing and associating outcome expectations with aversive stimuli could result in failure to plan and adjust future behaviour. In light of these findings, our observations of orbitofrontal under-activation to angry faces in ASD suggest that atypical integration of information concerning punishment, and difficulty deriving social averseness from angry faces, could contribute to social impairment in ASD. This is consistent with observations that anger processing recruits additional neural areas, supporting the idea that anger requires more resources and contextual information to respond appropriately (Lindner \u0026 Rosén, 2006; Pichon et al., 2009). It is interesting to note a lack of orbitofrontal activity differences between adolescents with and without ASD to happy faces, which may be due to reduced need for behavioural adaptation, and mediation following perception of positive emotion. This contrast may explain why adolescents with ASD, with their reduced processing of angry faces, show difficulties in recognizing and interpreting anger.\n\n4.2.3 Atypical angular gyrus activation in ASD to happy faces\nThe angular gyrus is a multi-modal hub that is implicated in a variety of functions, including playing a key role in mentalizing and social cognition (see Seghier, 2013 for a review). This model of the angular gyrus as a central hub of information processing coupled with our findings of atypical angular gyrus activation in ASD suggests a deficit in integrating and coordinating multiple cognitive domains, which manifests in affective processing difficulties. In adolescents with ASD, early left angular over-activation was followed by subsequent underactivation to happy faces, relative to controls. Left angular activation in controls to happy faces versus non-emotional stimuli (Habel et al., 2005) or neutral faces (Trautmann et al., 2009) has been observed, an effect that was not seen when shown negative faces. Angular gyrus activation for happy faces specifically is consistent with our data as there were differences in angular gyrus activation between adolescents with and without ASD to happy faces only.\n\n4.2.4 Lateralization of atypical temporal activation in ASD\nTemporal lobe areas are implicated in face processing and visuospatial processing (see Haxby et al., 2000 for a review). In response to viewing angry faces, a pattern of overactivation in the left middle and inferior temporal regions in ASD was noted, as well as underactivation in the right homologous temporal areas. Group effects in laterality were also seen in response to happy faces, with greater left superior, middle, and inferior temporal activation in ASD while the controls showed greater right inferior and middle temporal activation.\nCortical lateralization for specific types of information processing is often seen, such as language and visuo-spatial specialization in the left and right hemispheres, respectively. Stemming from lesion, electrophysiological and neuroimaging findings, the right hemisphere model/hypothesis of emotional processing posits a right cortical specialization for emotional processing (e.g., McLaren \u0026 Bryson, 1987), in contrast to a valence-specific bias, where implicit emotional processing in particular has hemispheric lateralization with the right hemisphere dominant for negative emotions (e.g., Sato \u0026 Aoki, 2006). A meta-analysis favoured the notion of a complex ‘emotional brain’ that encompasses bilateral neural regions (Demaree et al., 2005; Fusar-Poli et al., 2009) and other papers have also shown that the two models need to be considered (Smith \u0026 Bulman-Fleming, 2005). Few studies have investigated cortical specialization during emotional processing in ASD. Children with and without ASD have shown comparable right hemispheric advantage for perception of emotional expression of prosody (Baker et al., 2010). Adults with ASD showed a left visual field bias for affective faces, similarly to controls, but also showed a left visual bias in non-social conditions and on a task judging facial identity, which was not observed in controls (Ashwin et al., 2005). Our findings of consistently greater left hemisphere activity and reduced right activation in the temporal regions to affective faces in ASD suggest that their difficulties in affective processing may be attributable to increased left hemispheric lateralization at the expense of typical right hemispheric or bilateral processing.\nLastly, reduced right inferior temporal activation to happy faces was noted from 150 to 250 ms, in the time window associated with the M170/N170, a component typically showing greater amplitudes in the right hemisphere, sensitive to face processing and facial affect (Batty \u0026 Taylor, 2003; Bentin et al., 1996; Hung et al., 2010). Thus, these results suggest that atypical processing during this time window may contribute to impairments in processing happy faces in adolescents with ASD.\n\n4.2.5 Left insula underactivation in ASD to happy faces\nThe insulae, well connected to other limbic structures such as the amygdalae and the orbitofrontal cortices, are activated in response to a range of emotional processes (Duerden et al., 2013; Fusar-Poli et al., 2009; Sprengelmeyer et al., 1998). Given the key role of the insulae in emotional processing, left insula under-activation to happy faces in adolescents with ASD is consistent with the insensitivity towards social reward derived from happy faces shown in individuals with ASD. This highlights that despite the relative ease with which happy expressions are recognized in individuals with ASD, cognitive mechanisms underlying happy face processing in ASD remain impaired (Farran et al., 2011), and corroborates findings of social reward deficits as the insulae have extensive effective connectivity with the nucleus accumbens, a vital structure involved in reward processing (Breiter et al., 2001; Craig, 2003; Menon \u0026 Levitin, 2005).\n\n4.2.6 Conclusions\nThe present study demonstrated differences in the spatiotemporal properties of neural activity during happy and angry face processing in adolescents with ASD. Our findings show discrepant neural recruitment patterns in adolescents with ASD, particularly in their failure to adequately integrate frontal, temporal, tempo-parietal and limbic brain regions into the facial affect processing network. These results suggest that impairments in face processing and possible deficits in appreciating social reward and punishment from positive and negative faces, respectively, may play a role in facial affect processing deficits in adolescents with ASD.\nAs the period of adolescence is accompanied by marked affective changes, a peak in the prevalence of negative emotional states, and heightened and more variable emotional responses, future longitudinal studies examining the neural networks recruited during emotional face processing in clinical child and adult populations can determine if these group differences increase or decrease from childhood through adolescence and into adulthood (Compas et al., 1995; Hare et al., 2008). Such findings will be critical to understanding when in development this skill acquisition is disturbed. Characterizing the developmental trajectory of emotional face processing in ASD will ultimately contribute to the understanding of the processes that underlie social impairment in ASD. 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