PMC:4300004 / 2222-14817 JSONTXT

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Introduction\nEmotional face processing is an innate and universal ability that is integral to the acquisition of social skills (Ekman \u0026 Friesen, 1971; Meltzoff \u0026 Moore, 1977). The human face is the most important visual stimulus for human social interactions. The ability to extract the significance of expressive faces is critical for successful social interactions, as it facilitates the understanding of another's mental states and intentions and is important in guiding appropriate reciprocal behaviour. Impaired social functioning is one of the diagnostic hallmarks of Autism Spectrum Disorder (ASD). While it is generally understood that individuals with ASD experience difficulties with social cues, the current literature on emotional face processing in ASD has yielded inconsistent results with some studies finding deficits in emotional processing (e.g., Celani et al., 1999; Eack et al., 2014; García-Villamisar et al., 2010; Golan et al., 2008), with impairment in fear (Ashwin et al., 2007; Howard et al., 2000; Pelphrey et al., 2002), surprise (Baron-Cohen et al., 1993) and anger processing (Kuusikko et al., 2009), while others have noted no deficits (Adolphs et al., 2001; Balconi \u0026 Carrera, 2007; Buitelaar et al., 1999; Castelli, 2005; Tracy et al., 2011).\nIn typical development, emotional face processing is associated with activation in a widespread neural network, encompassing the visual, limbic, temporal, temporoparietal and prefrontal regions (Blair et al., 1999; Fusar-Poli et al., 2009; Phillips et al., 1999; Vuilleumier \u0026 Pourtois, 2007). The processing of happy facial expressions implicates a number of structures including the amygdalae, insulae, cingulate, inferior, medial and middle frontal, fusiform and middle temporal areas (Breiter et al., 1996; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Hoehl et al., 2010; Kesler-West et al., 2001; Phillips et al., 1998; Thomas et al., 2001). Angry faces elicit cingulate, bilateral fusiform, inferior frontal, superior temporal, middle and medial superior frontal, and orbitofrontal activity (Blair et al., 1999; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Kesler-West et al., 2001); moreover, decreased activation to angry, relative to neutral, faces has been found in the caudate nucleus, superior temporal, anterior cingulate (ACC), and medial frontal regions (Phillips et al., 1999). While the amygdalae have been widely reported to be involved in threat processing, amygdala activation to angry faces has not been found consistently (e.g., Phillips et al., 1999; Luo et al., 2007; Whalen et al., 2001; but see Fusar-Poli et al., 2009).\nAtypical activation of the social brain networks using fMRI during emotional face processing has been found in adults with ASD, including reduced left amygdala and orbitofrontal activation (Ashwin et al., 2007), greater activity in the left superior temporal gyrus and right peristriate visual cortex (Critchley et al., 2000), and reduced fusiform and extrastriate activity, while also showing activation comparable to controls in the anterior cingulate, superior temporal, medial frontal and insula regions (Deeley et al., 2007). Children and adolescents with ASD have shown reduced fusiform but greater precuneus activity during an emotion-matching task, but not during a simpler emotion labelling task (Wang et al., 2004). Collectively, these studies suggest that task demands modulate neural activity during emotional processing to a greater extent in individuals with ASD, and have likely contributed to the discrepant findings in existing literature (Wang et al., 2004).\nOf the two major subsystems involved in social cognition, the ventral orbitofrontal-amygdala circuit is of particular relevance to ASD as it is implicated in socio-emotional regulation and behaviour through the processing of others' emotional states, responses and intentions (see Bachevalier \u0026 Loveland, 2006, for a review). The orbitofrontal cortex contributes to this subsystem by mediating emotional behaviour, social inhibition, reversal learning and altering of unsuitable behaviour (Blair et al., 1999; Dias et al., 1996; Elliott et al., 2000; Rolls, 2004; Van Honk et al., 2005) as well deriving positive social joy and reward (Britton et al., 2006; Morris \u0026 Dolan, 2001). Sharing a close functional and anatomical reciprocal interconnection with the orbitofrontal cortex, atypical activation in the left amygdala during affect processing has been noted in ASD (e.g., Corbett et al., 2009; Critchley et al., 2000). Hence, focusing on the orbitofrontal-amygdala circuit dysfunction may aid in delineating the profile of facial affect processing in ASD.\n\n1.1 The spatiotemporal profile of neural activity during affect processing in ASD\nThere are few studies on the timing of the neural processing of emotional faces in ASD. ERP studies have noted variously a delay, reduced, or lack of activity in children and adults with ASD, relative to controls (Batty et al., 2011; Dawson et al., 2004; McPartland et al., 2004; O'Connor et al., 2005; Wong et al., 2008). A recent ERP study found that adolescents with ASD failed to show emotion-specific responses that were observed in the typically developing group (Wagner et al., 2013). Further, while face scanning was significantly associated with patterns of neural activation during face processing in typically developing adolescents, no such association was found in ASD (Wagner et al., 2013). Significant impairments in emotion recognition in adult, but not child, faces have also been noted in adolescents with ASD (Lerner et al., 2013). The same study also reported a significant association between the latency of the face-sensitive N170 component, localized to the fusiform gyri and inferior temporal areas, and deficits in emotion recognition in adolescents with ASD.\nOne study that investigated affective processing in adolescents with ASD using magnetoencephalography (MEG), which provides both timing and more accurate spatial information than EEG studies (Hari et al., 2010), showed reduced early emotion-specific gamma-band power, relative to controls, as well as later decreased power across all emotions (Wright et al., 2012). There do not appear to be other studies that have taken advantage of the spatio-temporal precision of MEG to determine the timing and/or brain regional activation differences in developmental ASD populations with emotional faces.\n\n1.2 Anger processing\nWhile emotional facial expressions of fear and anger both constitute threat-relevant signals, angry faces are more appropriate than fearful faces for investigating emotional face processing in ASD. Processing of anger requires the understanding of social norms and context, topics with which individuals with ASD struggle (Berkowitz, 1999; Zeman \u0026 Garber, 1996). Angry facial expressions are also more likely to be produced in response to repeated aggravations rather than first-time behavioural transgressions (Averill, 1982). Given that individuals with ASD are often poor at recognizing others' mental states or social norms, they have likely encountered displays of anger without understanding the implications (Bal et al., 2010; Baron-Cohen et al., 1999; Begeer et al., 2006). Past studies have specifically noted atypical angry facial processing in individuals with ASD (Ashwin et al., 2006; Kuusikko et al., 2009; Rieff et al., 2007; Rump et al., 2009). Age-effects in anger processing have also been noted, as older children and adolescents are able to correctly identify angry faces more often than younger children, regardless of diagnosis (Lindner \u0026 Rosén, 2006). There are also sharp increases in anger-specific sensitivity from adolescence to adulthood, providing support for a later maturation of anger processing (Thomas et al., 2007).\nAn fMRI study contrasting activations elicited by fear and anger in typical individuals showed that while both emotions activated a network of regions similarly, including the amygdalae and insulae, anger specifically elicited neural activation in a wider set of regions including the ventromedial prefrontal cortex and the posterior orbitofrontal cortex (Pichon et al., 2009). These areas have been implicated in behavioural regulation, supporting the idea that anger processing requires more resources and contextual information to adjust behaviour accordingly (Pichon et al., 2009).\n\n1.3 Happiness processing in ASD\nHappiness is the only one of the six basic emotions that is definitely positive and is the first emotion to be accurately identified in early development (Markham \u0026 Adams, 1992). Seemingly typical processing of happy affect in individuals with ASD has been observed, which may be due to the greater frequency of encountering and hence greater familiarity with happy faces (Critchley et al., 2000; Farran et al., 2011). However, while happy faces are socially rewarding for typically developing individuals (Phillips et al., 1998), insensitivity towards social reward derived from happy faces has been shown in individuals with ASD (Sepeta et al., 2012). Hence, it is important to investigate the underlying neural processes involved in the processing of happy faces in ASD to determine whether social reward systems are appropriately activated.\n\n1.4 Adolescence\nIn typically developing individuals, recognition of emotional face expressions follows a protracted developmental trajectory that extends into late adolescence (e.g., Batty \u0026 Taylor, 2006; Kolb et al., 1992). Asynchronous development of emotion recognition is well established (De Sonneville et al., 2002; Pichon et al., 2009) and neuroimaging findings have demonstrated the shifting involvement of different neural networks over the course of development (Hung et al., 2012; Killgore \u0026 Yurgelun-Todd, 2007; Monk et al., 2003; Thomas et al., 2001). At around 11 years of age emotional processing abilities undergo marked improvement, which would implicate greater demands on neural processes involved in emotional processing in early adolescence (Tonks et al., 2007).\nThere are few studies on emotional face processing in adolescents with ASD, representing a serious gap in the literature, as adolescence is a period of vulnerability, volatility and increased stress (Spear, 2000) during which the prevalence of negative emotions peaks and shows greater variability (Compas et al., 1995; Hare et al., 2008). Behavioural studies investigating emotional face processing in adolescents with ASD have shown affective processing comparable to controls (Grossman et al., 2000; Rieffe et al., 2007). Adolescents with ASD in these studies showed deficits in decoding emotions from static and dynamic facial affect overall, and, although they have been shown to identify specific emotions (Rump et al., 2009) such as happiness and sadness readily, they have difficulties with more complex emotions such as embarrassment (Capps et al., 1992) and identifying emotions when shown videos (Koning \u0026 Magill-Evans, 2001). Individuals with Asperger Syndrome but not high-functioning autism have shown intact emotion perception (Mazefsky \u0026 Oswald, 2007).\nAdults with ASD continue to experience difficulties when presented with brief or subtle emotions, and may never reach the same level of competency in emotional processing as typically developing adults (Begeer et al., 2006; Rieffe et al., 2007). The impairment in emotional processing in adults with ASD is consistent with the notion that individuals with ASD require compensatory strategies to achieve average performance. Although competency with emotional recognition in ASD improves with age, this skill often plateaus at a performance level below that of typically developing peers, or is associated with atypical brain activations to achieve comparable performance levels. These results underscore the need to examine the adolescent period of emotional processing in ASD to obtain a clearer understanding of the emotional development in this population.\nThus, the present study explored the neural substrates of implicit emotional face processing in adolescents with ASD using MEG, providing both temporal and spatial measures of brain processes, focusing on the neural areas implicated in emotional processing. We hypothesized that adolescents with ASD would show (1) shorter response latencies to emotional faces as they are not distracted by the emotions and (2) reduced and delayed patterns of neural activation in the frontal, limbic and temporal areas, key constituents of the social brain.\n"}

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Introduction\nEmotional face processing is an innate and universal ability that is integral to the acquisition of social skills (Ekman \u0026 Friesen, 1971; Meltzoff \u0026 Moore, 1977). The human face is the most important visual stimulus for human social interactions. The ability to extract the significance of expressive faces is critical for successful social interactions, as it facilitates the understanding of another's mental states and intentions and is important in guiding appropriate reciprocal behaviour. Impaired social functioning is one of the diagnostic hallmarks of Autism Spectrum Disorder (ASD). While it is generally understood that individuals with ASD experience difficulties with social cues, the current literature on emotional face processing in ASD has yielded inconsistent results with some studies finding deficits in emotional processing (e.g., Celani et al., 1999; Eack et al., 2014; García-Villamisar et al., 2010; Golan et al., 2008), with impairment in fear (Ashwin et al., 2007; Howard et al., 2000; Pelphrey et al., 2002), surprise (Baron-Cohen et al., 1993) and anger processing (Kuusikko et al., 2009), while others have noted no deficits (Adolphs et al., 2001; Balconi \u0026 Carrera, 2007; Buitelaar et al., 1999; Castelli, 2005; Tracy et al., 2011).\nIn typical development, emotional face processing is associated with activation in a widespread neural network, encompassing the visual, limbic, temporal, temporoparietal and prefrontal regions (Blair et al., 1999; Fusar-Poli et al., 2009; Phillips et al., 1999; Vuilleumier \u0026 Pourtois, 2007). The processing of happy facial expressions implicates a number of structures including the amygdalae, insulae, cingulate, inferior, medial and middle frontal, fusiform and middle temporal areas (Breiter et al., 1996; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Hoehl et al., 2010; Kesler-West et al., 2001; Phillips et al., 1998; Thomas et al., 2001). Angry faces elicit cingulate, bilateral fusiform, inferior frontal, superior temporal, middle and medial superior frontal, and orbitofrontal activity (Blair et al., 1999; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Kesler-West et al., 2001); moreover, decreased activation to angry, relative to neutral, faces has been found in the caudate nucleus, superior temporal, anterior cingulate (ACC), and medial frontal regions (Phillips et al., 1999). While the amygdalae have been widely reported to be involved in threat processing, amygdala activation to angry faces has not been found consistently (e.g., Phillips et al., 1999; Luo et al., 2007; Whalen et al., 2001; but see Fusar-Poli et al., 2009).\nAtypical activation of the social brain networks using fMRI during emotional face processing has been found in adults with ASD, including reduced left amygdala and orbitofrontal activation (Ashwin et al., 2007), greater activity in the left superior temporal gyrus and right peristriate visual cortex (Critchley et al., 2000), and reduced fusiform and extrastriate activity, while also showing activation comparable to controls in the anterior cingulate, superior temporal, medial frontal and insula regions (Deeley et al., 2007). Children and adolescents with ASD have shown reduced fusiform but greater precuneus activity during an emotion-matching task, but not during a simpler emotion labelling task (Wang et al., 2004). Collectively, these studies suggest that task demands modulate neural activity during emotional processing to a greater extent in individuals with ASD, and have likely contributed to the discrepant findings in existing literature (Wang et al., 2004).\nOf the two major subsystems involved in social cognition, the ventral orbitofrontal-amygdala circuit is of particular relevance to ASD as it is implicated in socio-emotional regulation and behaviour through the processing of others' emotional states, responses and intentions (see Bachevalier \u0026 Loveland, 2006, for a review). The orbitofrontal cortex contributes to this subsystem by mediating emotional behaviour, social inhibition, reversal learning and altering of unsuitable behaviour (Blair et al., 1999; Dias et al., 1996; Elliott et al., 2000; Rolls, 2004; Van Honk et al., 2005) as well deriving positive social joy and reward (Britton et al., 2006; Morris \u0026 Dolan, 2001). Sharing a close functional and anatomical reciprocal interconnection with the orbitofrontal cortex, atypical activation in the left amygdala during affect processing has been noted in ASD (e.g., Corbett et al., 2009; Critchley et al., 2000). Hence, focusing on the orbitofrontal-amygdala circuit dysfunction may aid in delineating the profile of facial affect processing in ASD.\n\n1.1 The spatiotemporal profile of neural activity during affect processing in ASD\nThere are few studies on the timing of the neural processing of emotional faces in ASD. ERP studies have noted variously a delay, reduced, or lack of activity in children and adults with ASD, relative to controls (Batty et al., 2011; Dawson et al., 2004; McPartland et al., 2004; O'Connor et al., 2005; Wong et al., 2008). A recent ERP study found that adolescents with ASD failed to show emotion-specific responses that were observed in the typically developing group (Wagner et al., 2013). Further, while face scanning was significantly associated with patterns of neural activation during face processing in typically developing adolescents, no such association was found in ASD (Wagner et al., 2013). Significant impairments in emotion recognition in adult, but not child, faces have also been noted in adolescents with ASD (Lerner et al., 2013). The same study also reported a significant association between the latency of the face-sensitive N170 component, localized to the fusiform gyri and inferior temporal areas, and deficits in emotion recognition in adolescents with ASD.\nOne study that investigated affective processing in adolescents with ASD using magnetoencephalography (MEG), which provides both timing and more accurate spatial information than EEG studies (Hari et al., 2010), showed reduced early emotion-specific gamma-band power, relative to controls, as well as later decreased power across all emotions (Wright et al., 2012). There do not appear to be other studies that have taken advantage of the spatio-temporal precision of MEG to determine the timing and/or brain regional activation differences in developmental ASD populations with emotional faces.\n\n1.2 Anger processing\nWhile emotional facial expressions of fear and anger both constitute threat-relevant signals, angry faces are more appropriate than fearful faces for investigating emotional face processing in ASD. Processing of anger requires the understanding of social norms and context, topics with which individuals with ASD struggle (Berkowitz, 1999; Zeman \u0026 Garber, 1996). Angry facial expressions are also more likely to be produced in response to repeated aggravations rather than first-time behavioural transgressions (Averill, 1982). Given that individuals with ASD are often poor at recognizing others' mental states or social norms, they have likely encountered displays of anger without understanding the implications (Bal et al., 2010; Baron-Cohen et al., 1999; Begeer et al., 2006). Past studies have specifically noted atypical angry facial processing in individuals with ASD (Ashwin et al., 2006; Kuusikko et al., 2009; Rieff et al., 2007; Rump et al., 2009). Age-effects in anger processing have also been noted, as older children and adolescents are able to correctly identify angry faces more often than younger children, regardless of diagnosis (Lindner \u0026 Rosén, 2006). There are also sharp increases in anger-specific sensitivity from adolescence to adulthood, providing support for a later maturation of anger processing (Thomas et al., 2007).\nAn fMRI study contrasting activations elicited by fear and anger in typical individuals showed that while both emotions activated a network of regions similarly, including the amygdalae and insulae, anger specifically elicited neural activation in a wider set of regions including the ventromedial prefrontal cortex and the posterior orbitofrontal cortex (Pichon et al., 2009). These areas have been implicated in behavioural regulation, supporting the idea that anger processing requires more resources and contextual information to adjust behaviour accordingly (Pichon et al., 2009).\n\n1.3 Happiness processing in ASD\nHappiness is the only one of the six basic emotions that is definitely positive and is the first emotion to be accurately identified in early development (Markham \u0026 Adams, 1992). Seemingly typical processing of happy affect in individuals with ASD has been observed, which may be due to the greater frequency of encountering and hence greater familiarity with happy faces (Critchley et al., 2000; Farran et al., 2011). However, while happy faces are socially rewarding for typically developing individuals (Phillips et al., 1998), insensitivity towards social reward derived from happy faces has been shown in individuals with ASD (Sepeta et al., 2012). Hence, it is important to investigate the underlying neural processes involved in the processing of happy faces in ASD to determine whether social reward systems are appropriately activated.\n\n1.4 Adolescence\nIn typically developing individuals, recognition of emotional face expressions follows a protracted developmental trajectory that extends into late adolescence (e.g., Batty \u0026 Taylor, 2006; Kolb et al., 1992). Asynchronous development of emotion recognition is well established (De Sonneville et al., 2002; Pichon et al., 2009) and neuroimaging findings have demonstrated the shifting involvement of different neural networks over the course of development (Hung et al., 2012; Killgore \u0026 Yurgelun-Todd, 2007; Monk et al., 2003; Thomas et al., 2001). At around 11 years of age emotional processing abilities undergo marked improvement, which would implicate greater demands on neural processes involved in emotional processing in early adolescence (Tonks et al., 2007).\nThere are few studies on emotional face processing in adolescents with ASD, representing a serious gap in the literature, as adolescence is a period of vulnerability, volatility and increased stress (Spear, 2000) during which the prevalence of negative emotions peaks and shows greater variability (Compas et al., 1995; Hare et al., 2008). Behavioural studies investigating emotional face processing in adolescents with ASD have shown affective processing comparable to controls (Grossman et al., 2000; Rieffe et al., 2007). Adolescents with ASD in these studies showed deficits in decoding emotions from static and dynamic facial affect overall, and, although they have been shown to identify specific emotions (Rump et al., 2009) such as happiness and sadness readily, they have difficulties with more complex emotions such as embarrassment (Capps et al., 1992) and identifying emotions when shown videos (Koning \u0026 Magill-Evans, 2001). Individuals with Asperger Syndrome but not high-functioning autism have shown intact emotion perception (Mazefsky \u0026 Oswald, 2007).\nAdults with ASD continue to experience difficulties when presented with brief or subtle emotions, and may never reach the same level of competency in emotional processing as typically developing adults (Begeer et al., 2006; Rieffe et al., 2007). The impairment in emotional processing in adults with ASD is consistent with the notion that individuals with ASD require compensatory strategies to achieve average performance. Although competency with emotional recognition in ASD improves with age, this skill often plateaus at a performance level below that of typically developing peers, or is associated with atypical brain activations to achieve comparable performance levels. These results underscore the need to examine the adolescent period of emotional processing in ASD to obtain a clearer understanding of the emotional development in this population.\nThus, the present study explored the neural substrates of implicit emotional face processing in adolescents with ASD using MEG, providing both temporal and spatial measures of brain processes, focusing on the neural areas implicated in emotional processing. We hypothesized that adolescents with ASD would show (1) shorter response latencies to emotional faces as they are not distracted by the emotions and (2) reduced and delayed patterns of neural activation in the frontal, limbic and temporal areas, key constituents of the social brain.\n"}

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Introduction\nEmotional face processing is an innate and universal ability that is integral to the acquisition of social skills (Ekman \u0026 Friesen, 1971; Meltzoff \u0026 Moore, 1977). The human face is the most important visual stimulus for human social interactions. The ability to extract the significance of expressive faces is critical for successful social interactions, as it facilitates the understanding of another's mental states and intentions and is important in guiding appropriate reciprocal behaviour. Impaired social functioning is one of the diagnostic hallmarks of Autism Spectrum Disorder (ASD). While it is generally understood that individuals with ASD experience difficulties with social cues, the current literature on emotional face processing in ASD has yielded inconsistent results with some studies finding deficits in emotional processing (e.g., Celani et al., 1999; Eack et al., 2014; García-Villamisar et al., 2010; Golan et al., 2008), with impairment in fear (Ashwin et al., 2007; Howard et al., 2000; Pelphrey et al., 2002), surprise (Baron-Cohen et al., 1993) and anger processing (Kuusikko et al., 2009), while others have noted no deficits (Adolphs et al., 2001; Balconi \u0026 Carrera, 2007; Buitelaar et al., 1999; Castelli, 2005; Tracy et al., 2011).\nIn typical development, emotional face processing is associated with activation in a widespread neural network, encompassing the visual, limbic, temporal, temporoparietal and prefrontal regions (Blair et al., 1999; Fusar-Poli et al., 2009; Phillips et al., 1999; Vuilleumier \u0026 Pourtois, 2007). The processing of happy facial expressions implicates a number of structures including the amygdalae, insulae, cingulate, inferior, medial and middle frontal, fusiform and middle temporal areas (Breiter et al., 1996; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Hoehl et al., 2010; Kesler-West et al., 2001; Phillips et al., 1998; Thomas et al., 2001). Angry faces elicit cingulate, bilateral fusiform, inferior frontal, superior temporal, middle and medial superior frontal, and orbitofrontal activity (Blair et al., 1999; Devinsky et al., 1995; Fusar-Poli et al., 2009; García-Villamisar et al., 2010; Kesler-West et al., 2001); moreover, decreased activation to angry, relative to neutral, faces has been found in the caudate nucleus, superior temporal, anterior cingulate (ACC), and medial frontal regions (Phillips et al., 1999). While the amygdalae have been widely reported to be involved in threat processing, amygdala activation to angry faces has not been found consistently (e.g., Phillips et al., 1999; Luo et al., 2007; Whalen et al., 2001; but see Fusar-Poli et al., 2009).\nAtypical activation of the social brain networks using fMRI during emotional face processing has been found in adults with ASD, including reduced left amygdala and orbitofrontal activation (Ashwin et al., 2007), greater activity in the left superior temporal gyrus and right peristriate visual cortex (Critchley et al., 2000), and reduced fusiform and extrastriate activity, while also showing activation comparable to controls in the anterior cingulate, superior temporal, medial frontal and insula regions (Deeley et al., 2007). Children and adolescents with ASD have shown reduced fusiform but greater precuneus activity during an emotion-matching task, but not during a simpler emotion labelling task (Wang et al., 2004). Collectively, these studies suggest that task demands modulate neural activity during emotional processing to a greater extent in individuals with ASD, and have likely contributed to the discrepant findings in existing literature (Wang et al., 2004).\nOf the two major subsystems involved in social cognition, the ventral orbitofrontal-amygdala circuit is of particular relevance to ASD as it is implicated in socio-emotional regulation and behaviour through the processing of others' emotional states, responses and intentions (see Bachevalier \u0026 Loveland, 2006, for a review). The orbitofrontal cortex contributes to this subsystem by mediating emotional behaviour, social inhibition, reversal learning and altering of unsuitable behaviour (Blair et al., 1999; Dias et al., 1996; Elliott et al., 2000; Rolls, 2004; Van Honk et al., 2005) as well deriving positive social joy and reward (Britton et al., 2006; Morris \u0026 Dolan, 2001). Sharing a close functional and anatomical reciprocal interconnection with the orbitofrontal cortex, atypical activation in the left amygdala during affect processing has been noted in ASD (e.g., Corbett et al., 2009; Critchley et al., 2000). Hence, focusing on the orbitofrontal-amygdala circuit dysfunction may aid in delineating the profile of facial affect processing in ASD.\n\n1.1 The spatiotemporal profile of neural activity during affect processing in ASD\nThere are few studies on the timing of the neural processing of emotional faces in ASD. ERP studies have noted variously a delay, reduced, or lack of activity in children and adults with ASD, relative to controls (Batty et al., 2011; Dawson et al., 2004; McPartland et al., 2004; O'Connor et al., 2005; Wong et al., 2008). A recent ERP study found that adolescents with ASD failed to show emotion-specific responses that were observed in the typically developing group (Wagner et al., 2013). Further, while face scanning was significantly associated with patterns of neural activation during face processing in typically developing adolescents, no such association was found in ASD (Wagner et al., 2013). Significant impairments in emotion recognition in adult, but not child, faces have also been noted in adolescents with ASD (Lerner et al., 2013). The same study also reported a significant association between the latency of the face-sensitive N170 component, localized to the fusiform gyri and inferior temporal areas, and deficits in emotion recognition in adolescents with ASD.\nOne study that investigated affective processing in adolescents with ASD using magnetoencephalography (MEG), which provides both timing and more accurate spatial information than EEG studies (Hari et al., 2010), showed reduced early emotion-specific gamma-band power, relative to controls, as well as later decreased power across all emotions (Wright et al., 2012). There do not appear to be other studies that have taken advantage of the spatio-temporal precision of MEG to determine the timing and/or brain regional activation differences in developmental ASD populations with emotional faces.\n\n1.2 Anger processing\nWhile emotional facial expressions of fear and anger both constitute threat-relevant signals, angry faces are more appropriate than fearful faces for investigating emotional face processing in ASD. Processing of anger requires the understanding of social norms and context, topics with which individuals with ASD struggle (Berkowitz, 1999; Zeman \u0026 Garber, 1996). Angry facial expressions are also more likely to be produced in response to repeated aggravations rather than first-time behavioural transgressions (Averill, 1982). Given that individuals with ASD are often poor at recognizing others' mental states or social norms, they have likely encountered displays of anger without understanding the implications (Bal et al., 2010; Baron-Cohen et al., 1999; Begeer et al., 2006). Past studies have specifically noted atypical angry facial processing in individuals with ASD (Ashwin et al., 2006; Kuusikko et al., 2009; Rieff et al., 2007; Rump et al., 2009). Age-effects in anger processing have also been noted, as older children and adolescents are able to correctly identify angry faces more often than younger children, regardless of diagnosis (Lindner \u0026 Rosén, 2006). There are also sharp increases in anger-specific sensitivity from adolescence to adulthood, providing support for a later maturation of anger processing (Thomas et al., 2007).\nAn fMRI study contrasting activations elicited by fear and anger in typical individuals showed that while both emotions activated a network of regions similarly, including the amygdalae and insulae, anger specifically elicited neural activation in a wider set of regions including the ventromedial prefrontal cortex and the posterior orbitofrontal cortex (Pichon et al., 2009). These areas have been implicated in behavioural regulation, supporting the idea that anger processing requires more resources and contextual information to adjust behaviour accordingly (Pichon et al., 2009).\n\n1.3 Happiness processing in ASD\nHappiness is the only one of the six basic emotions that is definitely positive and is the first emotion to be accurately identified in early development (Markham \u0026 Adams, 1992). Seemingly typical processing of happy affect in individuals with ASD has been observed, which may be due to the greater frequency of encountering and hence greater familiarity with happy faces (Critchley et al., 2000; Farran et al., 2011). However, while happy faces are socially rewarding for typically developing individuals (Phillips et al., 1998), insensitivity towards social reward derived from happy faces has been shown in individuals with ASD (Sepeta et al., 2012). Hence, it is important to investigate the underlying neural processes involved in the processing of happy faces in ASD to determine whether social reward systems are appropriately activated.\n\n1.4 Adolescence\nIn typically developing individuals, recognition of emotional face expressions follows a protracted developmental trajectory that extends into late adolescence (e.g., Batty \u0026 Taylor, 2006; Kolb et al., 1992). Asynchronous development of emotion recognition is well established (De Sonneville et al., 2002; Pichon et al., 2009) and neuroimaging findings have demonstrated the shifting involvement of different neural networks over the course of development (Hung et al., 2012; Killgore \u0026 Yurgelun-Todd, 2007; Monk et al., 2003; Thomas et al., 2001). At around 11 years of age emotional processing abilities undergo marked improvement, which would implicate greater demands on neural processes involved in emotional processing in early adolescence (Tonks et al., 2007).\nThere are few studies on emotional face processing in adolescents with ASD, representing a serious gap in the literature, as adolescence is a period of vulnerability, volatility and increased stress (Spear, 2000) during which the prevalence of negative emotions peaks and shows greater variability (Compas et al., 1995; Hare et al., 2008). Behavioural studies investigating emotional face processing in adolescents with ASD have shown affective processing comparable to controls (Grossman et al., 2000; Rieffe et al., 2007). Adolescents with ASD in these studies showed deficits in decoding emotions from static and dynamic facial affect overall, and, although they have been shown to identify specific emotions (Rump et al., 2009) such as happiness and sadness readily, they have difficulties with more complex emotions such as embarrassment (Capps et al., 1992) and identifying emotions when shown videos (Koning \u0026 Magill-Evans, 2001). Individuals with Asperger Syndrome but not high-functioning autism have shown intact emotion perception (Mazefsky \u0026 Oswald, 2007).\nAdults with ASD continue to experience difficulties when presented with brief or subtle emotions, and may never reach the same level of competency in emotional processing as typically developing adults (Begeer et al., 2006; Rieffe et al., 2007). The impairment in emotional processing in adults with ASD is consistent with the notion that individuals with ASD require compensatory strategies to achieve average performance. Although competency with emotional recognition in ASD improves with age, this skill often plateaus at a performance level below that of typically developing peers, or is associated with atypical brain activations to achieve comparable performance levels. These results underscore the need to examine the adolescent period of emotional processing in ASD to obtain a clearer understanding of the emotional development in this population.\nThus, the present study explored the neural substrates of implicit emotional face processing in adolescents with ASD using MEG, providing both temporal and spatial measures of brain processes, focusing on the neural areas implicated in emotional processing. We hypothesized that adolescents with ASD would show (1) shorter response latencies to emotional faces as they are not distracted by the emotions and (2) reduced and delayed patterns of neural activation in the frontal, limbic and temporal areas, key constituents of the social brain.\n"}