Abstract Background Scanning faces is important for social interactions. Difficulty with the social use of eye contact constitutes one of the clinical symptoms of autism spectrum disorder (ASD). It has been suggested that individuals with ASD look less at the eyes and more at the mouth than typically developing (TD) individuals, possibly due to gaze aversion or gaze indifference. However, eye-tracking evidence for this hypothesis is mixed. While gaze patterns convey information about overt orienting processes, it is unclear how this is manifested at the neural level and how relative covert attention to the eyes and mouth of faces might be affected in ASD. Methods We used frequency-tagging EEG in combination with eye tracking, while participants watched fast flickering faces for 1-min stimulation sequences. The upper and lower halves of the faces were presented at 6 Hz and 7.5 Hz or vice versa in different stimulation sequences, allowing to objectively disentangle the neural saliency of the eyes versus mouth region of a perceived face. We tested 21 boys with ASD (8–12 years old) and 21 TD control boys, matched for age and IQ. Results Both groups looked longer at the eyes than the mouth, without any group difference in relative fixation duration to these features. TD boys looked significantly more to the nose, while the ASD boys looked more outside the face. EEG neural saliency data partly followed this pattern: neural responses to the upper or lower face half were not different between groups, but in the TD group, neural responses to the lower face halves were larger than responses to the upper part. Face exploration dynamics showed that TD individuals mostly maintained fixations within the same facial region, whereas individuals with ASD switched more often between the face parts. Limitations Replication in large and independent samples may be needed to validate exploratory results. Conclusions Combined eye-tracking and frequency-tagged neural responses show no support for the excess mouth/diminished eye gaze hypothesis in ASD. The more exploratory face scanning style observed in ASD might be related to their increased feature-based face processing style.
This study tested the extent to which there are neural correlates of the influence of affective personality information on face processing, using event-related potentials (ERPs). In the learning phase, participants viewed a target individual's face (with a neutral expression or faint smile) paired with negative, neutral or positive sentences describing the target's previous typical behavior. In the following EEG testing phase, participants completed gender judgments of the learned faces. Statistical analyses were conducted on measures of neural activity during the gender judgment task. Repeated measures ANOVA of ERP data showed that faces described as having a negative personality elicited larger N170 than did those with a neutral or positive description. The early posterior negativity (EPN) showed the same pattern, with larger amplitudes for faces paired with negative personality than for others. The size of the late positive potential (LPP) was larger for faces paired with positive personality than for those with neutral and negative personality. The current study indicates that affective personality information is associated with an automatic, top-down modulation of face processing.
The human brain is frequently exposed to individual faces across a wide range of different apparent sizes, often seen simultaneously (e.g., when facing a crowd). Here we used a sensitive and objective fast periodic visual stimulation approach while recording scalp electroencephalogram (EEG) to test the effect of size variation on neural responses reflecting individual face discrimination. EEG was recorded in ten observers presented with the same face identity at a fixed rate (5.88 Hz, frequency F) and different oddball face identities appearing every five faces (F/5, i.e., 1.18 Hz). Stimulus size was either constant (6.5 × 4 degrees of visual angle) or changed randomly at each stimulation cycle, by 2:1 ratio increasing values from 10% to 80% size variation in four conditions. Absolute stimulus size remained constant across conditions. The base rate 5.88 Hz EEG response increased with image size variation, particularly over the right occipito-temporal cortex. In contrast, size variation decreased the oddball response marking individual face discrimination over the right occipito-temporal cortex. At constant stimulus size, the F/5 change of identity generated an early (about 100 ms) oddball response reflecting individual face discrimination based on image-based cues. This early component disappeared with a relatively small size variation (i.e., 20%), leaving a robust high-level index of individual face discrimination. Stimulus size variation is an important manipulation to isolate the contribution of high-level visual processes to individual face discrimination. Nevertheless, even for relatively small stimuli, high-level individual face discrimination processes in the right occipito-temporal cortex remain sensitive to stimulus size variation.
Decisions of attractiveness from the human face are made instantly and spontaneously, but robust implicit neural measures of facial attractiveness discrimination are currently lacking. Here we applied fast periodic visual stimulation coupled with electroencephalography (EEG) to objectively measure the neural coding of facial attractiveness. We presented different pictures of faces at 6 Hz, i.e. six faces/second, for a minute while participants attended to a central fixation cross and indicated whether the cross shortly changed color. Every other face in the stimulation was attractive and was replaced by a relatively less attractive face. This resulted in alternating more/less attractive faces at a 3 Hz rate, eliciting a significant increase in occipito-temporal EEG amplitude at 3 Hz both at the group and the individual participant level. This response was absent in two control conditions where either only attractive or only less attractive faces were presented. These observations support the view that face-sensitive visual areas discriminate attractiveness implicitly and rapidly from the human face.
A key aspect of human individual face recognition is the ability to discriminate unfamiliar individual faces. Since many general processes contribute to explicit behavioural performance in individual face discrimination tasks, measuring unfamiliar individual face discrimination ability in humans is challenging. In recent years, a fast periodic visual stimulation approach has provided objective (frequency-locked) implicit electrophysiological indices of individual face discrimination that are highly sensitive at the individual level. Here we evaluate the test-retest reliability of this response across scalp electroencephalographic (EEG) recording sessions separated by more than two months, in the same 30 individuals. We found no test-retest difference overall across sessions in terms of amplitude and spatial distribution of the EEG individual face discrimination response. Moreover, with only 4 minutes of recordings, the variable individual face discrimination response across individuals was highly stable (i.e., reliable) in terms of amplitude, spatial distribution and shape. This stable EEG response was also significantly correlated with speed, but not accuracy rate, of the Benton face recognition task (BFRT-c, Rossion, & Michel, 2018). Overall, these observations strengthen the diagnostic value of FPVS-EEG as an objective and rapid flag for specific difficulties at individual face recognition in the human population. Rossion, B., & Michel, C. (2017). Normative data for accuracy and response times at the computerized Benton Facial Recognition Test (BFRT-c). Behavior Research Methods
We objectively quantified the neural sensitivity of school-aged boys with and without autism spectrum disorder (ASD) to detect briefly presented fearful expressions by combining fast periodic visual stimulation with frequency-tagging electroencephalography. Images of neutral faces were presented at 6 Hz, periodically interleaved with fearful expressions at 1.2 Hz oddball rate. While both groups equally display the face inversion effect and mainly rely on information from the mouth to detect fearful expressions, boys with ASD generally show reduced neural responses to rapid changes in expression. At an individual level, fear discrimination responses predict clinical status with an 83% accuracy. This implicit and straightforward approach identifies subtle deficits that remain concealed in behavioral tasks, thereby opening new perspectives for clinical diagnosis.
Abstract Difficulties in automatic emotion processing in individuals with autism spectrum disorder (ASD) might remain concealed in behavioral studies due to compensatory strategies. To gain more insight in the mechanisms underlying facial emotion recognition, we recorded eye tracking and facial mimicry data of 20 school‐aged boys with ASD and 20 matched typically developing controls while performing an explicit emotion recognition task. Proportional looking times to specific face regions (eyes, nose, and mouth) and face exploration dynamics were analyzed. In addition, facial mimicry was assessed. Boys with ASD and controls were equally capable to recognize expressions and did not differ in proportional looking times, and number and duration of fixations. Yet, specific facial expressions elicited particular gaze patterns, especially within the control group. Both groups showed similar face scanning dynamics, although boys with ASD demonstrated smaller saccadic amplitudes. Regarding the facial mimicry, we found no emotion specific facial responses and no group differences in the responses to the displayed facial expressions. Our results indicate that boys with and without ASD employ similar eye gaze strategies to recognize facial expressions. Smaller saccadic amplitudes in boys with ASD might indicate a less exploratory face processing strategy. Yet, this slightly more persistent visual scanning behavior in boys with ASD does not imply less efficient emotion information processing, given the similar behavioral performance. Results on the facial mimicry data indicate similar facial responses to emotional faces in boys with and without ASD. Lay Summary We investigated (i) whether boys with and without autism apply different face exploration strategies when recognizing facial expressions and (ii) whether they mimic the displayed facial expression to a similar extent. We found that boys with and without ASD recognize facial expressions equally well, and that both groups show similar facial reactions to the displayed facial emotions. Yet, boys with ASD visually explored the faces slightly less than the boys without ASD.
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