Preserved action recognition in children with autism spectrum disorders: Evidence from an EEG and eye-tracking study.

Individuals with Autism Spectrum Disorder (ASD) have difficulties recognizing and understanding others' actions. The goal of the present study was to determine whether children with and without ASD show differences in the way they process stimuli depicting Biological Motion (BM). Thirty-two children aged 7-16 (16 ASD and 16 typically developing (TD) controls) participated in two experiments. In the first experiment, electroencephalography (EEG) was used to record low (8-10 Hz) and high (10-13 Hz) mu and beta (15-25 Hz) bands during the observation three different Point Light Displays (PLD) of action. In the second experiment, participants answered to action-recognition tests and their accuracy and response time were recorded, together with their eye-movements. There were no group differences in EEG data (first experiment), indicating that children with and without ASD do not differ in their mu suppression (8-13 Hz) and beta activity (15-25 Hz). However, behavioral data from second experiment revealed that children with ASD were less accurate and slower than TD children in their responses to an action recognition task. In addition, eye-tracking data indicated that children with ASD paid less attention to the body compared to the background when watching PLD stimuli. Our results indicate that the more the participants focused on the PLDs, the more they displayed mu suppressions. These results could challenge the results of previous studies that had not controlled for visual attention and found a possible deficit in MNS functions of individuals with ASD. We discuss possible mechanisms and interpretations.

The EU-Emotion Voice Database.

In this study, we report the validation results of the EU-Emotion Voice Database, an emotional voice database available for scientific use, containing a total of 2,159 validated emotional voice stimuli. The EU-Emotion voice stimuli consist of audio-recordings of 54 actors, each uttering sentences with the intention of conveying 20 different emotional states (plus neutral). The database is organized in three separate emotional voice stimulus sets in three different languages (British English, Swedish, and Hebrew). These three sets were independently validated by large pools of participants in the UK, Sweden, and Israel. Participants' validation of the stimuli included emotion categorization accuracy and ratings of emotional valence, intensity, and arousal. Here we report the validation results for the emotional voice stimuli from each site and provide validation data to download as a supplement, so as to make these data available to the scientific community. The EU-Emotion Voice Database is part of the EU-Emotion Stimulus Set, which in addition contains stimuli of emotions expressed in the visual modality (by facial expression, body language, and social scene) and is freely available to use for academic research purposes.

Influence of anxiety and alexithymia on brain activations associated with the perception of others' pain in autism.

The circumstances under which empathy is altered in ASD remain unclear, as previous studies did not systematically find differences in brain activation between ASD and controls in empathy-eliciting paradigms, and did not always monitor whether differences were primarily due to ASD "per se", or to conditions overlapping with ASD, such as alexithymia and anxiety. Here, we collected fMRI data from 47 participants (22 ASD) viewing pictures depicting hands and feet of unknown others in painful, disgusting, or neutral situations. We computed brain activity for painful and disgusting stimuli (vs. neutral) in whole brain and in regions of interest among the brain areas typically activated during the perception of nociceptive stimuli. Group differences in brain activation disappeared when either alexithymia or anxiety - both elevated in the ASD group - were controlled for. Regression analyses indicated that the influence of symptoms was mainly shared between autistic symptomatology, alexithymia and anxiety or driven by unique contributions from alexithymia or anxiety. Our results suggest that affective empathy may be affected in ASD, but that this association is complex. The respective contribution of alexithymia and anxiety to decreased affective empathy of people with ASD may be due to the association of those psychiatric conditions with reduced motor resonance/Theory of Mind.

Emotional expression in psychiatric conditions: New technology for clinicians.

AIM: Emotional expressions are one of the most widely studied topics in neuroscience, from both clinical and non-clinical perspectives. Atypical emotional expressions are seen in various psychiatric conditions, including schizophrenia, depression, and autism spectrum conditions. Understanding the basics of emotional expressions and recognition can be crucial for diagnostic and therapeutic procedures. Emotions can be expressed in the face, gesture, posture, voice, and behavior and affect physiological parameters, such as the heart rate or body temperature. With modern technology, clinicians can use a variety of tools ranging from sophisticated laboratory equipment to smartphones and web cameras. The aim of this paper is to review the currently used tools using modern technology and discuss their usefulness as well as possible future directions in emotional expression research and treatment strategies. METHODS: The authors conducted a literature review in the PubMed, EBSCO, and SCOPUS databases, using the following key words: 'emotions,' 'emotional expression,' 'affective computing,' and 'autism.' The most relevant and up-to-date publications were identified and discussed. Search results were supplemented by the authors' own research in the field of emotional expression. RESULTS: We present a critical review of the currently available technical diagnostic and therapeutic methods. The most important studies are summarized in a table. CONCLUSION: Most of the currently available methods have not been adequately validated in clinical settings. They may be a great help in everyday practice; however, they need further testing. Future directions in this field include more virtual-reality-based and interactive interventions, as well as development and improvement of humanoid robots.

Effect of visual stimuli of pain on empathy brain network in people with and without Autism Spectrum Disorder.

The extent to which affective empathy is impaired in Autism Spectrum Disorder (ASD) remains unclear, as some-but not all-previous neuroimaging studies investigating empathy for pain in ASD have shown similar activation levels to those of neurotypicals individuals. These inconsistent results could be due to the use of different empathy-eliciting stimuli. While some studies used pictures of faces exhibiting a painful expression, others used pictures of limbs in painful situations. In this study, we used fMRI to compare activation in areas associated with empathy processing (empathy network) for these two types of stimuli in 31 participants (16 with ASD, 15 controls). We found a group difference in the inferior frontal gyrus (IFG) and the thalamus when participants viewed stimuli of limbs in painful situations, but not when they viewed face stimuli with a painful expression. Both groups of participants activated their empathy network more when viewing pictures of limbs in painful situations than when viewing pictures of faces with a painful expression; this increased activation for limbs versus faces was significantly enhanced in controls relative to ASD participants, especially in the secondary somatosensory cortex (SII). Our findings suggest that empathy defect of people with ASD is contingent upon the type of stimuli used, and may be related to the level of Mirror Neuron System involvement, as brain regions showing group differences (IFG, SII) underlie embodiment. We discuss the potential clinical implications of our findings in terms of developing interventions boosting the empathetic abilities of people with ASD.

Bumetanide for autism: more eye contact, less amygdala activation.

We recently showed that constraining eye contact leads to exaggerated increase of amygdala activation in autism. Here, in a proof of concept pilot study, we demonstrate that administration of bumetanide (a NKCC1 chloride importer antagonist that restores GABAergic inhibition) normalizes the level of amygdala activation during constrained eye contact with dynamic emotional face stimuli in autism. In addition, eye-tracking data reveal that bumetanide administration increases the time spent in spontaneous eye gaze during in a free-viewing mode of the same face stimuli. In keeping with clinical trials, our data support the Excitatory/Inhibitory dysfunction hypothesis in autism, and indicate that bumetanide may improve specific aspects of social processing in autism. Future double-blind placebo controlled studies with larger cohorts of participants will help clarify the mechanisms of bumetanide action in autism.

Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes.

Previous studies that showed decreased brain activation in people with autism spectrum disorder (ASD) viewing expressive faces did not control that participants looked in the eyes. This is problematic because ASD is characterized by abnormal attention to the eyes. Here, we collected fMRI data from 48 participants (27 ASD) viewing pictures of neutral faces and faces expressing anger, happiness, and fear at low and high intensity, with a fixation cross between the eyes. Group differences in whole brain activity were examined for expressive faces at high and low intensity versus neutral faces. Group differences in neural activity were also investigated in regions of interest within the social brain, including the amygdala and the ventromedial prefrontal cortex (vmPFC). In response to low intensity fearful faces, ASD participants showed increased activation in the social brain regions, and decreased functional coupling between the amygdala and the vmPFC. This oversensitivity to low intensity fear coupled with a lack of emotional regulation capacity could indicate an excitatory/inhibitory imbalance in their socio-affective processing system. This may result in social disengagement and avoidance of eye-contact to handle feelings of strong emotional reaction. Our results also demonstrate the importance of careful control of gaze when investigating emotional processing in ASD. Hum Brain Mapp 38:5943-5957, 2017. © 2017 Wiley Periodicals, Inc.

Look me in the eyes: constraining gaze in the eye-region provokes abnormally high subcortical activation in autism.

Individuals with Autism Spectrum Disorder (ASD) seem to have difficulties looking others in the eyes, but the substrate for this behavior is not well understood. The subcortical pathway, which consists of superior colliculus, pulvinar nucleus of the thalamus, and amygdala, enables rapid and automatic face processing. A specific component of this pathway - i.e., the amygdala - has been shown to be abnormally activated in paradigms where individuals had to specifically attend to the eye-region; however, a direct examination of the effect of manipulating the gaze to the eye-regions on all the components of the subcortical system altogether has never been performed. The subcortical system is particularly important as it shapes the functional specialization of the face-processing cortex during development. Using functional MRI, we investigated the effect of constraining gaze in the eye-region during dynamic emotional face perception in groups of participants with ASD and typical controls. We computed differences in activation in the subcortical face processing system (superior colliculus, pulvinar nucleus of the thalamus and amygdala) for the same stimuli seen freely or with the gaze constrained in the eye-region. Our results show that when constrained to look in the eyes, individuals with ASD show abnormally high activation in the subcortical system, which may be at the basis of their eye avoidance in daily life.

The effect of constraining eye-contact during dynamic emotional face perception-an fMRI study.

Eye-contact modifies how we perceive emotions and modulates activity in the social brain network. Here, using fMRI, we demonstrate that adding a fixation cross in the eye region of dynamic facial emotional stimuli significantly increases activation in the social brain of healthy, neurotypical participants when compared with activation for the exact same stimuli observed in a free-viewing mode. In addition, using PPI analysis, we show that the degree of amygdala connectivity with the rest of the brain is enhanced for the constrained view for all emotions tested except for fear, and that anxiety and alexithymia modulate the strength of amygdala connectivity for each emotion differently. Finally, we show that autistic traits have opposite effects on amygdala connectivity for fearful and angry emotional expressions, suggesting that these emotions should be treated separately in studies investigating facial emotion processing.

Basic and complex emotion recognition in children with autism: cross-cultural findings.

BACKGROUND: Children with autism spectrum conditions (ASC) have emotion recognition deficits when tested in different expression modalities (face, voice, body). However, these findings usually focus on basic emotions, using one or two expression modalities. In addition, cultural similarities and differences in emotion recognition patterns in children with ASC have not been explored before. The current study examined the similarities and differences in the recognition of basic and complex emotions by children with ASC and typically developing (TD) controls across three cultures: Israel, Britain, and Sweden. METHODS: Fifty-five children with high-functioning ASC, aged 5-9, were compared to 58 TD children. On each site, groups were matched on age, sex, and IQ. Children were tested using four tasks, examining recognition of basic and complex emotions from voice recordings, videos of facial and bodily expressions, and emotional video scenarios including all modalities in context. RESULTS: Compared to their TD peers, children with ASC showed emotion recognition deficits in both basic and complex emotions on all three modalities and their integration in context. Complex emotions were harder to recognize, compared to basic emotions for the entire sample. Cross-cultural agreement was found for all major findings, with minor deviations on the face and body tasks. CONCLUSIONS: Our findings highlight the multimodal nature of ER deficits in ASC, which exist for basic as well as complex emotions and are relatively stable cross-culturally. Cross-cultural research has the potential to reveal both autism-specific universal deficits and the role that specific cultures play in the way empathy operates in different countries.

An investigation of the 'female camouflage effect' in autism using a computerized ADOS-2 and a test of sex/gender differences.

BACKGROUND: Autism spectrum conditions (autism) are diagnosed more frequently in boys than in girls. Females with autism may have been under-identified due to not only a male-biased understanding of autism but also females' camouflaging. The study describes a new technique that allows automated coding of non-verbal mode of communication (gestures) and offers the possibility of objective, evaluation of gestures, independent of human judgment. The EyesWeb software platform and the Kinect sensor during two demonstration activities of ADOS-2 (Autism Diagnostic Observation Schedule, Second Edition) were used. METHODS: The study group consisted of 33 high-functioning Polish girls and boys with formal diagnosis of autism or Asperger syndrome aged 5-10, with fluent speech, IQ average and above and their parents (girls with autism, n = 16; boys with autism, n = 17). All children were assessed during two demonstration activities of Module 3 of ADOS-2, administered in Polish, and coded using Polish codes. Children were also assessed with Polish versions of the Eyes and Faces Tests. Parents provided information on the author-reviewed Polish research translation of SCQ (Social Communication Questionnaire, Current and Lifetime) and Polish version of AQ Child (Autism Spectrum Quotient, Child). RESULTS: Girls with autism tended to use gestures more vividly as compared to boys with autism during two demonstration activities of ADOS-2. Girls with autism made significantly more mistakes than boys with autism on the Faces Test. All children with autism had high scores in AQ Child, which confirmed the presence of autistic traits in this group. The current communication skills of boys with autism reported by parents in SCQ were significantly better than those of girls with autism. However, both girls with autism and boys with autism improved in the social and communication abilities over the lifetime. The number of stereotypic behaviours in boys significantly decreased over life whereas it remained at a comparable level in girls with autism. CONCLUSIONS: High-functioning females with autism might present better on non-verbal (gestures) mode of communication than boys with autism. It may camouflage other diagnostic features. It poses risk of under-diagnosis or not receiving the appropriate diagnosis for this population. Further research is required to examine this phenomenon so appropriate gender revisions to the diagnostic assessments might be implemented.

Autistic traits influence gaze-oriented attention to happy but not fearful faces.

The relationship between autistic traits and gaze-oriented attention to fearful and happy faces was investigated at the behavioral and neuronal levels. Upright and inverted dynamic face stimuli were used in a gaze-cueing paradigm while event related potentials (ERPs) were recorded. Participants responded faster to gazed-at than to non-gazed-at targets, and this gaze orienting effect (GOE) diminished with inversion, suggesting it relies on facial configuration. It was also larger for fearful than happy faces but only in participants with high autism-spectrum quotient (AQ) scores. While the GOE to fearful faces was of similar magnitude regardless of AQ scores, a diminished GOE to happy faces was found in participants with high AQ scores. At the ERP level, a congruency effect on target-elicited P1 component reflected enhanced visual processing of gazed-at targets. In addition, cue-triggered early directing attention negativity and anterior directing attention negativity reflected, respectively, attention orienting and attention holding at gazed-at locations. These neural markers of spatial attention orienting were not modulated by emotion and were not found in participants with high AQ scores. Together, these findings suggest that autistic traits influence attention orienting to gaze and its modulation by social emotions such as happiness.

EMOTIONAL MODULATION OF ATTENTION ORIENTING BY GAZE VARIES WITH DYNAMIC CUE SEQUENCE.

Recent gaze cueing studies using dynamic cue sequences have reported increased attention orienting by gaze with faces expressing fear, surprise or anger. Here, we investigated whether the type of dynamic cue sequence used impacted the magnitude of this effect. When the emotion was expressed before or concurrently with gaze shift, no modulation of gaze-oriented attention by emotion was seen. In contrast, when the face cue averted gaze before expressing an emotion (as if reacting to the object after first localizing it), the gaze orienting effect was clearly increased for fearful, surprised and angry faces compared to neutral faces. Thus, the type of dynamic sequence used, and in particular the order in which the gaze shift and the facial expression are presented, modulate gaze-oriented attention, with maximal modulation seen when the expression of emotion follows gaze shift.

Fearful, surprised, happy, and angry facial expressions modulate gaze-oriented attention: behavioral and ERP evidence.

The impact of emotions on gaze-oriented attention was investigated in non-anxious participants. A neutral face cue with straight gaze was presented, which then averted its gaze to the side while remaining neutral or expressing an emotion (fear/surprise in Exp.1 and anger/happiness in Exp.2). Localization of a subsequent target was faster at the gazed-at location (congruent condition) than at the non-gazed-at location (incongruent condition). This Gaze-Orienting Effect (GOE) was enhanced for fear, surprise, and anger, compared to neutral expressions which did not differ from happy expressions. In addition, Event Related Potentials (ERPs) to the target showed a congruency effect on P1 for fear and surprise and a left lateralized congruency effect on P1 for happy faces, suggesting that target visual processing was also influenced by attention to gaze and emotions. Finally, at cue presentation, early postero-lateral (Early Directing Attention Negativity (EDAN)) and later antero-lateral (Anterior Directing Attention Negativity (ADAN)) attention-related ERP components were observed, reflecting, respectively, the shift of attention and its holding at gazed-at locations. These two components were not modulated by emotions. Together, these findings show that the processing of social signals such as gaze and facial expression interact rather late and in a complex manner to modulate spatial attention.