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Enhanced Early Visual Responses During Implicit Emotional Faces Processing in Autism Spectrum Disorder

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Research on Autism Spectrum Disorder (ASD) has focused on processing of socially-relevant stimuli, such as faces. Nonetheless, before being ‘social’, faces are visual stimuli. The present magnetoencephalography study investigated the time course of brain activity during an implicit emotional task in visual emotion-related regions in 19 adults with ASD (mean age 26.3 ± 4.4) and 19 typically developed controls (26.4 ± 4). The results confirmed previously-reported differences between groups in brain responses to emotion and a hypo-activation in the ASD group in the right fusiform gyrus around 150 ms. However, the ASD group also presented early enhanced activity in the occipital region. These results support that impaired face processing in ASD might be sustained by atypical responses in primary visual areas.
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Vol.:(0123456789)
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Journal of Autism and Developmental Disorders (2019) 49:871–886
https://doi.org/10.1007/s10803-018-3787-3
ORIGINAL PAPER
Enhanced Early Visual Responses During Implicit Emotional Faces
Processing inAutism Spectrum Disorder
KlaraKovarski1,2 · RoccoMennella2,3· SimeonM.Wong2,4· BenjaminT.Dunkley2,4,5· MargotJ.Taylor2,4,5,6·
MagaliBatty7
Published online: 29 October 2018
© Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
Research on Autism Spectrum Disorder (ASD) has focused on processing of socially-relevant stimuli, such as faces. None-
theless, before being ‘social’, faces are visual stimuli. The present magnetoencephalography study investigated the time
course of brain activity during an implicit emotional task in visual emotion-related regions in 19 adults with ASD (mean age
26.3 ± 4.4) and 19 typically developed controls (26.4 ± 4). The results confirmed previously-reported differences between
groups in brain responses to emotion and a hypo-activation in the ASD group in the right fusiform gyrus around 150ms.
However, the ASD group also presented early enhanced activity in the occipital region. These results support that impaired
face processing in ASD might be sustained by atypical responses in primary visual areas.
Keywords Autism· MEG· Face processing· Emotion· Visual processing
Autism Spectrum Disorder (ASD) is a neurodevelopmental
disorder characterized by two major groups of behavioural
symptoms. The first includes difficulties in the social and
communication area and the second is defined by restricted
interests and stereotyped behaviours. However, atypicalities
in all sensory modalities are now considered as core symp-
toms of autism (APA 2013; Marco etal. 2011). In the visual
domain, hyper and hypo-responsiveness to external stim-
uli, as well as unusual visuo-motor behaviours, including
abnormal scanning or auto-stimulation, are often observed
from infancy (Mottron etal. 2007; Simmons etal. 2009).
Enhanced perception of details, as well as difficulties in pro-
cessing the global picture, are often reported to account for
such atypical strategies and behaviours (Happé and Frith
2006; Mottron etal. 2006).
In line with general difficulties for ASD in processing
the significant flow of sensory information in the environ-
ment (Gomot and Wicker 2012), facial expressions are
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s1080 3-018-3787-3) contains
supplementary material, which is available to authorized users.
* Klara Kovarski
klara.kovarski@gmail.com
Rocco Mennella
Rocco.mennella@gmail.com
Simeon M. Wong
simeon.wong@sickkids.ca
Benjamin T. Dunkley
ben.dunkley@sickkids.ca
Margot J. Taylor
margot.taylor@sickkids.ca
Magali Batty
magali.batty@univ-tlse2.fr
1 UMR 1253, iBrain, Université de Tours, Inserm, Centre
Universitaire de PédoPsychiatrie, Tours, France
2 Department ofDiagnostic Imaging, The Hospital fortheSick
Children, Toronto, Canada
3 Laboratoire de neurosciences cognitives, INSERM U960,
Département d’études cognitives, École Normale Supérieure,
PSL Research University, Paris, France
4 Neurosciences & Mental Health Program, The Hospital
fortheSick Children Research Institute, Toronto, Canada
5 Department ofMedical Imaging, University ofToronto,
Toronto, Canada
6 Department ofPsychology, University ofToronto, Toronto,
Canada
7 Present Address: CERPPS, Université de Toulouse,
Toulouse, France
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Buttressing our results of decreasing connectivity in this gamma-based network with age in autism, task-based studies of emotional face processing have shown altered functional connectivity of the amygdalae in autism (Monk et al., 2010;Sato et al., 2019;Swartz et al., 2013). Of particular relevance, the fusiform gyri and amygdalae were shown to be recruited when facial expressions are perceived in an implicit manner (Critchley et al., 2000), and the engagement and functional connectivity of these regions were found to be reduced in adults with ASD during the implicit processing of emotional information, yet preserved for explicit processing (Kana et al., 2016;Kovarski et al., 2019;Wong et al., 2008). In the present study, reduced connectivity of the right fusiform gyrus and amygdala with age in ASD may reflect the disrupted or delayed maturation of well-established emotional face processing areas and their circuitry, while age-related increased functional connectivity in controls demonstrates the protracted development of connectivity of these regions into adulthood. ...
... The implicit task in this study entails automatic and rapid processing of facial expressions, where deficits in perception cannot be compensated by learned strategies and increased experience with age. This can be achieved for the explicit processing of emotions in ASD (Frith and Frith, 2008;Frith, 2004) and thus explicit emotion recognition can be relatively preserved (Kana et al., 2016;Kovarski et al., 2019). It will be important for future work to investigate the neurodevelopmental trajectory of explicit emotional face processing in those with the disorder. ...
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Impairments in social functioning are hallmarks of autism spectrum disorder (ASD) and atypical functional connectivity may underlie these difficulties. Emotion processing networks typically undergo protracted maturational changes, however, those with ASD show either hyper- or hypo-connectivity with little consensus on the functional connectivity underpinning emotion processing. Magnetoencephalography was used to investigate age-related changes in whole-brain functional connectivity of eight regions of interest during happy and angry face processing in 190 children, adolescents and adults (6-39 years) with and without ASD. Findings revealed age-related changes from child- through to mid-adulthood in functional connectivity in controls and in ASD in theta, as well as age-related between-group differences across emotions, with connectivity decreasing in ASD, but increasing for controls, in gamma. Greater connectivity to angry faces was observed across groups in gamma. Emotion-specific age-related between-group differences in beta were also found, that showed opposite trends with age for happy and angry in ASD. Our results establish altered, frequency-specific developmental trajectories of functional connectivity in ASD, across distributed networks and a broad age range, which may finally help explain the heterogeneity in the literature.
... MEG has not been previously leveraged to investigate functional connectivity in NDDs and TD individuals; thus, the current MEG study is the first to investigate functional connectivity during the implicit presentation of happy and angry faces in ASD, ADHD and TD groups. Greater difficulties in emotion processing may be seen when tasks are implicit vs. explicit (Wong et al., 2008;Kana et al., 2016;Luckhardt et al., 2017); alterations in neural activation in ASD using implicit emotion processing tasks are widely reported (Critchley et al., 2000b;Batty et al., 2011;Leung et al., 2015Leung et al., , 2018Leung et al., , 2019Kana et al., 2016;Mennella et al., 2017;Kovarski et al., 2019). Difficulties in implicit emotion processing are thought to be due to the subconscious, rapid and automatic demands, while for explicit processing difficulties may be compensated for by learning strategies, experience and enhanced directed attention to faces (Frith, 2004;Begeer et al., 2006). ...
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Impairments in emotional face processing are demonstrated by individuals with neurodevelopmental disorders (NDDs), including autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), which is associated with altered emotion processing networks. Despite accumulating evidence of high rates of diagnostic overlap and shared symptoms between ASD and ADHD, functional connectivity underpinning emotion processing across these two neurodevelopmental disorders, compared to typical developing peers, has rarely been examined. The current study used magnetoencephalography to investigate whole-brain functional connectivity during the presentation of happy and angry faces in 258 children (5-19 years), including ASD, ADHD and typically developing (TD) groups to determine possible differences in emotion processing. Data-driven clustering was also applied to determine whether the patterns of connectivity differed among diagnostic groups. We found reduced functional connectivity in the beta band in ASD compared to TD, and a further reduction in the ADHD group compared to the ASD and the TD groups, across emotions. A group-by-emotion interaction in the gamma frequency band was also observed. Greater connectivity to happy compared to angry faces was found in the ADHD and TD groups, while the opposite pattern was seen in ASD. Data-driven subgrouping identified two distinct subgroups: NDD-dominant and TD-dominant; these subgroups demonstrated emotion-and frequency-specific differences in connectivity. Atypicalities in specific brain networks were strongly correlated with the severity of diagnosis-specific symptoms. Functional connectivity strength in the beta network was negatively correlated with difficulties in attention; in the gamma network, functional connectivity strength to happy faces was positively correlated with adaptive behavioural functioning, but in contrast, negatively correlated to angry faces. Our findings establish atypical frequency-and emotion-specific patterns of functional connectivity between NDD and TD children. Data-driven clustering further highlights a high degree of comorbidity and symptom overlap between the ASD and ADHD children.
... Activation within other task-activated visual regions, including V1 and MST, was unaffected in ASD, echoing our recent study in which response amplitudes were also normal within V1, but increased in early visual and dorsal visual regions (Martinez et al., 2019). Similar visual hypo/hyper activation patterns in Sz vs. ASD have been observed in both fMRI (reviewed in Samson et al., 2012; and electrophysiological (Martinez et al., 2018(Martinez et al., , 2019Shah et al., 2018;Kovarski et al., 2019) studies, supporting the concept that dysregulation of the early visual system may undermine later stages of visual processing. ...
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One important aspect for managing social interactions is the ability to perceive and respond to facial expressions rapidly and accurately. This ability is highly dependent upon intact processing within both cortical and subcortical components of the early visual pathways. Social cognitive deficits, including face emotion recognition (FER) deficits, are characteristic of several neuropsychiatric disorders including schizophrenia (Sz) and autism spectrum disorders (ASD). Here, we investigated potential visual sensory contributions to FER deficits in Sz (n = 28, 8/20 female/male; age 21-54 years) and adult ASD (n = 20, 4/16 female/male; age 19-43 years) participants compared to neurotypical (n = 30, 8/22 female/male; age 19-54 years) controls using task-based fMRI during an implicit static/dynamic FER task. Compared to neurotypical controls, both Sz (d = 1.97) and ASD (d = 1.13) participants had significantly lower FER scores which interrelated with diminished activation of the superior temporal sulcus (STS). In Sz, STS deficits were predicted by reduced activation of early visual regions (d = 0.85, p = 0.002) and of the pulvinar nucleus of the thalamus (d = 0.44, p = 0.042), along with impaired cortico-pulvinar interaction. By contrast, ASD participants showed patterns of increased early visual cortical (d = 1.03, p = 0.001) and pulvinar (d = 0.71, p = 0.015) activation. Large effect-size structural and histological abnormalities of pulvinar have previously been documented in Sz. Moreover, we have recently demonstrated impaired pulvinar activation to simple visual stimuli in Sz. Here, we provide the first demonstration of a disease-specific contribution of impaired pulvinar activation to social cognitive impairment in Sz.
... A negative correlation was found between altered right FFG MRI measurements and fearful FER accuracy in patients with FSZ, especially altered mfALFF of the right FFG. A large number of studies have shown that the FFG is associated with FER in different disorders, including bipolar disorder (Bertocci et al. 2019), autism spectrum disorder (Kovarski et al. 2019), and traumatic brain injury (Rigon et al. 2019). The FFG, especially the right FFG, supports face processing, social communication, and facial identity processing (Pourtois et al. 2010). ...
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Our aim was to analyse the correlation between the fractional amplitude of low-frequency fluctuation (fALFF) and facial emotion recognition (FER) ability in patients with first-episode schizophrenia (FSZ). A total of 28 patients with FSZ and 33 healthy controls (HCs) completed visual search tasks for FER ability. Regions of interest (ROIs) related to facial emotion were obtained from a previous meta-analysis. Pearson correlation analysis was performed to understand the correlation between fALFF and FER ability. Our results indicated that the patients performed worse than the HCs in the accuracy performances of happy FER and fearful FER. The previous meta-analysis results showed that the brain regions related to FER included the bilateral amygdala (AMY)/hippocampus (HIP), right fusiform gyrus (FFG), and right supplementary motor area (SMA). Pearson correlation showed that the fALFF of the right FFG was associated with high-load fearful FER accuracy ( r = -0.43, p = 0.022). Multiple regression analysis showed that the fALFF of the right FFG was an independent contributor to fearful FER accuracy. Our study indicates that FER ability is correlated with resting-state intrinsic activity in brain regions related to facial emotion, which may provide a reference for the study of FER in schizophrenia.
... In a recent magnetoencephalography study, the ASD group presented early enhanced activity in the occipital region, suggesting that impaired face processing in ASD might be sustained by atypical responses in primary visual areas (Kovarski et al., 2019). Anecdotal experiences of individuals with ASD report overwhelming sensations of visual details in everyday environments that they cannot pass without becoming absorbed in them. ...
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Introduction There has been a growing effort to characterize the time‐varying functional connectivity of resting state (RS) fMRI brain networks (RSNs). Although voxel‐wise connectivity studies have examined different sliding window lengths, nonsequential volume‐wise approaches have been less common. Methods Inspired by earlier co‐activation pattern (CAP) studies, we applied hierarchical clustering (HC) to classify the image volumes of the RS‐fMRI data on 28 adolescents with autism spectrum disorder (ASD) and their 27 typically developing (TD) controls. We compared the distribution of the ASD and TD groups' volumes in CAPs as well as their voxel‐wise means. For simplification purposes, we conducted a group independent component analysis to extract 14 major RSNs. The RSNs' average z‐scores enabled us to meaningfully regroup the RSNs and estimate the percentage of voxels within each RSN for which there was a significant group difference. These results were jointly interpreted to find global group‐specific patterns. Results We found similar brain state proportions in 58 CAPs (clustering interval from 2 to 30). However, in many CAPs, the voxel‐wise means differed significantly within a matrix of 14 RSNs. The rest‐activated default mode‐positive and default mode‐negative brain state properties vary considerably in both groups over time. This division was seen clearly when the volumes were partitioned into two CAPs and then further examined along the HC dendrogram of the diversifying brain CAPs. The ASD group network activations followed a more heterogeneous distribution and some networks maintained higher baselines; throughout the brain deactivation state, the ASD participants had reduced deactivation in 12/14 networks. During default mode‐negative CAPs, the ASD group showed simultaneous visual network and either dorsal attention or default mode network overactivation. Conclusion Nonsequential volume gathering into CAPs and the comparison of voxel‐wise signal changes provide a complementary perspective to connectivity and an alternative to sliding window analysis.
... To test our hypothesis, we recorded evoked responses from adolescents with ASD and TD controls using MEG during implicit emotional face processing of happy and angry faces. So far, MEG investigations in individuals with ASD have studied exclusively the cerebral activity during emotional face processing (Bailey, Braeutigam, Jousmäki, & Swithenby, 2005;Kovarski et al., 2019;Leung et al., 2015;Leung, Pang, Anagnostou, & Taylor, 2018;Leung, Pang, Brian, & Taylor, 2019;Safar et al., 2020;Wright et al., 2012). Tracking the time windows in the millisecond range can provide insights on how the cerebellar activations in response to affective faces compare with the well-known cerebral mediators (i.e., insula, fusiform) of face processing, at well-studied latencies (i.e., N170, Bentin, Allison, Puce, Perez, & McCarthy, 1996). ...
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Autism spectrum disorder (ASD) is characterized by social deficits and atypical facial processing of emotional expressions. The underlying neuropathology of these abnormalities is still unclear. Recent studies implicate cerebellum in emotional processing; other studies show cerebellar abnormalities in ASD. Here, we elucidate the spatiotemporal activation of cerebellar lobules in ASD during emotional processing of happy and angry faces in adolescents with ASD and typically developing (TD) controls. Using magnetoencephalography, we calculated dynamic statistical parametric maps across a period of 500 ms after emotional stimuli onset and determined differences between group activity to happy and angry emotions. Following happy face presentation, adolescents with ASD exhibited only left-hemispheric cerebellar activation in a cluster extending from lobule VI to lobule V (compared to TD controls). Following angry face presentation, adolescents with ASD exhibited only midline cerebellar activation (posterior IX vermis). Our findings indicate an early (125-175 ms) overactivation in cerebellar activity only for happy faces and a later overactivation for both happy (250-450 ms) and angry (250-350 ms) faces in adolescents with ASD. The prioritized hemispheric activity (happy faces) could reflect the promotion of a more flexible and adaptive social behavior, while the latter midline activity (angry faces) may guide conforming behavior.
... Moreover, we showed that only the TD group displayed a greater response to the angry stimulus compared to the neutral one, while this modulation by the emotion was not observed in the ASD group 7,47 . These atypical sensory responses suggest that early steps of face and facial expression processing are altered in adults with ASD, in accordance with previous neuroimaging findings showing atypical responses in the occipito-temporal regions 6,[48][49][50] . As demonstrated by the increasing number of studies using vMMN paradigms in psychiatric neurodevelopmental and neurodegenerative conditions, vMMN component is considered as a potential electrophysiological marker of automatic change detection (for a review and meta-analysis, see ref. 21 ). ...
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Unusual behaviors and brain activity to socio-emotional stimuli have been reported in Autism Spectrum Disorder (ASD). Atypical reactivity to change and intolerance of uncertainty are also present, but little is known on their possible impact on facial expression processing in autism. The visual mismatch negativity (vMMN) is an electrophysiological response automatically elicited by changing events such as deviant emotional faces presented among regular neutral faces. While vMMN has been found altered in ASD in response to low-level changes in simple stimuli, no study has investigated this response to visual social stimuli. Here two deviant expressions were presented, neutral and angry, embedded in a sequence of repetitive neutral stimuli. vMMN peak analyses were performed for latency and amplitude in early and late time windows. The ASD group presented smaller amplitude of the late vMMN to both neutral and emotional deviants compared to the typically developed adults (TD) group, and only the TD group presented a sustained activity related to emotional change (i.e., angry deviant). Source reconstruction of the vMMNs further revealed that any change processing elicited a reduced activity in ASD group compared to TD in the saliency network, while the specific processing emotional change elicited activity in the temporal region and in the insula. This study confirms atypical change processing in ASD and points to a specific difficulty in the processing of emotional changes, potentially playing a crucial role in social interaction deficits. Nevertheless, these results require to be further replicated with a greater sample size and generalized to other emotional expressions.
... A large literature, including multiple meta-analyses, confirms that individuals with ASD show deficiencies in recognising emotion from facial displays [106,107]. The evidence also points towards a more general abnormality in face processing, including eye fixations [108] and neural activations when viewing faces [98,109,110]. When examined from a developmental perspective, these face processing deficits may result from a failure of the amygdala to automatically assign faces as salient throughout early development. ...
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Purpose of Review Individuals with autism spectrum disorder (ASD) have often been reported to demonstrate a range of anomalies in visual perceptual function. Rather than reflecting an epiphenomenon to core social communication difficulties in ASD, a visual disturbance in early development could provide a causal mechanism for some aspects of impaired social communication. An overview of key visual pathways and cortical/subcortical regions of the visual system is provided, to aid the reader in appreciating the subsequent discussion of the relationship between visual processing and social communication. Recent Findings We then outline the evidence for visual anomalies in ASD and propose that an impairment in an infant’s ability to quickly orient visual attention and to rapidly code the dynamics of non-verbal social cues—such as eye gaze and facial expression changes—could be critically important in the development of social skills. Summary Faces are a rich source of information about the emotions and mental states of people with whom we engage. Faces are also used to assess trustworthiness and to predict individual responses. Without rapid visual information processing, faces in particular could become confusing and mysterious. We conclude with some suggestions for future research into the visual contributions to social skills in ASD and argue that the speed of visual information processing—driven by the fast magnocellular ‘M’ channel—is a necessary first step for the development of the social skills associated with the understanding of facial communication cues.
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