Effect of Familiarity on Reward Anticipation in Children with and without Autism Spectrum Disorders

Background

Previous research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.

Methods

The stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.

Results

No significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.

Conclusions

The findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.     

Reduced Face Aftereffects in Autism Are Not Due to Poor Attention

This study aimed to determine why face identity aftereffects are diminished in children with autism, relative to typical children. To address the possibility that reduced face aftereffects might reflect reduced attention to adapting stimuli, we investigated the consequence of controlling attention to adapting faces during a face identity aftereffect task in children with autism and typical children. We also included a size-change between adaptation and test stimuli to determine whether the reduced aftereffects reflect atypical adaptation to low- or higher-level stimulus properties. Results indicated that when attention was controlled and directed towards adapting stimuli, face identity aftereffects in children with autism were significantly reduced relative to typical children. This finding challenges the notion that atypicalities in the quality and/or quantity of children’s attention during adaptation might account for group differences previously observed in this paradigm. Additionally, evidence of diminished face identity aftereffects despite a stimulus size change supports an adaptive processing atypicality in autism that extends beyond low-level, retinotopically coded stimulus properties. These findings support the notion that diminished face aftereffects in autism reflect atypicalities in adaptive norm-based coding, which could also contribute to face processing difficulties in this group.     

Adaptation improves discrimination of face identity

Whether face adaptation confers any advantages to perceptual processing remains an open question. We investigated whether face adaptation can enhance the ability to make fine discriminations in the vicinity of the adapted face. We compared face discrimination thresholds in three adapting conditions: (i) same-face: where adapting and test faces were the same, (ii) different-face: where adapting and test faces differed, and (iii) baseline: where the adapting stimulus was a blank. Discrimination thresholds for morphed identity changes involving the adapted face (same-face) improved compared with those from both the baseline (no-adaptation) and different-face conditions. Since adapting to a face did not alter discrimination performance for other faces, this effect is selective for the facial identity that is adapted. These results indicate a form of gain control to heighten perceptual sensitivity in the vicinity of a currently viewed face, analogous to forms of adaptive gain control at lower levels of the visual system.     

Impaired Eye Region Search Accuracy in Children with Autistic Spectrum Disorders

To explore mechanisms underlying reduced fixation of eyes in autism, children with Autistic Spectrum Disorders (ASD) and typically developing children were tested in five visual search experiments: simple color feature; color-shape conjunction; face in non-face objects; mouth region; and eye region. No group differences were found for reaction time profile shapes in any of the five experiments, suggesting intact basic search mechanics in children with ASD. Contrary to early reports in the literature, but consistent with other more recent findings, we observed no superiority for conjunction search in children with ASD. Importantly, children with ASD did show reduced accuracy for eye region search (p = .005), suggesting that eyes contribute less to high-level face representations in ASD or that there is an eye region-specific disruption to attentional processes engaged by search in ASD.     

Auditory adaptation in voice perception

Perceptual aftereffects following adaptation to simple stimulus attributes (e.g., motion, color) have been studied for hundreds of years. A striking recent discovery was that adaptation also elicits contrastive aftereffects in visual perception of complex stimuli and faces [1-6]. Here, we show for the first time that adaptation to nonlinguistic information in voices elicits systematic auditory aftereffects. Prior adaptation to male voices causes a voice to be perceived as more female (and vice versa), and these auditory aftereffects were measurable even minutes after adaptation. By contrast, crossmodal adaptation effects were absent, both when male or female first names and when silently articulating male or female faces were used as adaptors. When sinusoidal tones (with frequencies matched to male and female voice fundamental frequencies) were used as adaptors, no aftereffects on voice perception were observed. This excludes explanations for the voice aftereffect in terms of both pitch adaptation and postperceptual adaptation to gender concepts and suggests that contrastive voice-coding mechanisms may routinely influence voice perception. The role of adaptation in calibrating properties of high-level voice representations indicates that adaptation is not confined to vision but is a ubiquitous mechanism in the perception of nonlinguistic social information from both faces and voices.     

Gamma activation in young people with autism spectrum disorders and typically-developing controls when viewing emotions on faces

Background

Behavioural studies have highlighted irregularities in recognition of facial affect in children and young people with autism spectrum disorders (ASDs). Recent findings from studies utilising electroencephalography (EEG) and magnetoencephalography (MEG) have identified abnormal activation and irregular maintenance of gamma (>30 Hz) range oscillations when ASD individuals attempt basic visual and auditory tasks.

Methodology/Principal Fndings

The pilot study reported here is the first study to use spatial filtering techniques in MEG to explore face processing in children with ASD. We set out to examine theoretical suggestions that gamma activation underlying face processing may be different in a group of children and young people with ASD (n = 13) compared to typically developing (TD) age, gender and IQ matched controls. Beamforming and virtual electrode techniques were used to assess spatially localised induced and evoked activity. While lower-band (3–30 Hz) responses to faces were similar between groups, the ASD gamma response in occipital areas was observed to be largely absent when viewing emotions on faces. Virtual electrode analysis indicated the presence of intact evoked responses but abnormal induced activity in ASD participants.

Conclusions/Significance

These findings lend weight to previous suggestions that specific components of the early visual response to emotional faces is abnormal in ASD. Elucidation of the nature and specificity of these findings is worthy of further research.     

Abnormal FMRI adaptation to unfamiliar faces in a case of developmental prosopamnesia

In rare cases, damage to the temporal lobe causes a selective impairment in the ability to learn new faces, a condition known as prosopamnesia [1]. Here we present the case of an individual with prosopamnesia in the absence of any acquired structural lesion. "C" shows intact processing of simple and complex nonface objects, but her ability to learn new faces is severely impaired. We used a neural marker of perceptual learning known as repetition suppression to examine functioning within C's fusiform face area (FFA), a region of cortex involved in face perception [2]. For comparison, we examined repetition suppression in the scene-selective parahippocampal place area (PPA) [3]. As expected, normal controls showed significant region-specific attenuation of neural activity across repetitions of each stimulus class. C also showed normal attenuation within the PPA to familiar and unfamiliar scenes, and within the FFA to familiar faces. Critically, however, she failed to show any adaptive change within the FFA for repeated unfamiliar faces, despite a face-specific blood-oxygen-dependent response (BOLD) response in her FFA during viewing of face stimuli. Our findings suggest that in developmental prosopamnesia, the FFA cannot maintain stable representations of new faces for subsequent recall or recognition.     

Neural basis of self and other representation in autism: an FMRI study of self-face recognition

Background

Autism is a developmental disorder characterized by decreased interest and engagement in social interactions and by enhanced self-focus. While previous theoretical approaches to understanding autism have emphasized social impairments and altered interpersonal interactions, there is a recent shift towards understanding the nature of the representation of the self in individuals with autism spectrum disorders (ASD). Still, the neural mechanisms subserving self-representations in ASD are relatively unexplored.

Methodology/Principal Findings

We used event-related fMRI to investigate brain responsiveness to images of the subjects'' own face and to faces of others. Children with ASD and typically developing (TD) children viewed randomly presented digital morphs between their own face and a gender-matched other face, and made “self/other” judgments. Both groups of children activated a right premotor/prefrontal system when identifying images containing a greater percentage of the self face. However, while TD children showed activation of this system during both self- and other-processing, children with ASD only recruited this system while viewing images containing mostly their own face.

Conclusions/Significance

This functional dissociation between the representation of self versus others points to a potential neural substrate for the characteristic self-focus and decreased social understanding exhibited by these individuals, and suggests that individuals with ASD lack the shared neural representations for self and others that TD children and adults possess and may use to understand others.     

Luminance- and Texture-Defined Information Processing in School-Aged Children with Autism

According to the complexity-specific hypothesis, the efficacy with which individuals with autism spectrum disorder (ASD) process visual information varies according to the extensiveness of the neural network required to process stimuli. Specifically, adults with ASD are less sensitive to texture-defined (or second-order) information, which necessitates the implication of several cortical visual areas. Conversely, the sensitivity to simple, luminance-defined (or first-order) information, which mainly relies on primary visual cortex (V1) activity, has been found to be either superior (static material) or intact (dynamic material) in ASD. It is currently unknown if these autistic perceptual alterations are present in childhood. In the present study, behavioural (threshold) and electrophysiological measures were obtained for static luminance- and texture-defined gratings presented to school-aged children with ASD and compared to those of typically developing children. Our behavioural and electrophysiological (P140) results indicate that luminance processing is likely unremarkable in autistic children. With respect to texture processing, there was no significant threshold difference between groups. However, unlike typical children, autistic children did not show reliable enhancements of brain activity (N230 and P340) in response to texture-defined gratings relative to luminance-defined gratings. This suggests reduced efficiency of neuro-integrative mechanisms operating at a perceptual level in autism. These results are in line with the idea that visual atypicalities mediated by intermediate-scale neural networks emerge before or during the school-age period in autism.     

Visual adaptation and face perception

The appearance of faces can be strongly affected by the characteristics of faces viewed previously. These perceptual after-effects reflect processes of sensory adaptation that are found throughout the visual system, but which have been considered only relatively recently in the context of higher level perceptual judgements. In this review, we explore the consequences of adaptation for human face perception, and the implications of adaptation for understanding the neural-coding schemes underlying the visual representation of faces. The properties of face after-effects suggest that they, in part, reflect response changes at high and possibly face-specific levels of visual processing. Yet, the form of the after-effects and the norm-based codes that they point to show many parallels with the adaptations and functional organization that are thought to underlie the encoding of perceptual attributes like colour. The nature and basis for human colour vision have been studied extensively, and we draw on ideas and principles that have been developed to account for norms and normalization in colour vision to consider potential similarities and differences in the representation and adaptation of faces.     

Adaptor Identity Modulates Adaptation Effects in Familiar Face Identification and Their Neural Correlates

Adaptation-related aftereffects (AEs) show how face perception can be altered by recent perceptual experiences. Along with contrastive behavioural biases, modulations of the early event-related potentials (ERPs) were typically reported on categorical levels. Nevertheless, the role of the adaptor stimulus per se for face identity-specific AEs is not completely understood and was therefore investigated in the present study. Participants were adapted to faces (S1s) varying systematically on a morphing continuum between pairs of famous identities (identities A and B), or to Fourier phase-randomized faces, and had to match the subsequently presented ambiguous faces (S2s; 50/50% identity A/B) to one of the respective original faces. We found that S1s identical with or near to the original identities led to strong contrastive biases with more identity B responses following A adaptation and vice versa. In addition, the closer S1s were to the 50/50% S2 on the morphing continuum, the smaller the magnitude of the AE was. The relation between S1s and AE was, however, not linear. Additionally, stronger AEs were accompanied by faster reaction times. Analyses of the simultaneously recorded ERPs revealed categorical adaptation effects starting at 100 ms post-stimulus onset, that were most pronounced at around 125–240 ms for occipito-temporal sites over both hemispheres. S1-specific amplitude modulations were found at around 300–400 ms. Response-specific analyses of ERPs showed reduced voltages starting at around 125 ms when the S1 biased perception in a contrastive way as compared to when it did not. Our results suggest that face identity AEs do not only depend on physical differences between S1 and S2, but also on perceptual factors, such as the ambiguity of S1. Furthermore, short-term plasticity of face identity processing might work in parallel to object-category processing, and is reflected in the first 400 ms of the ERP.     

Orientation-contingent face aftereffects and implications for face-coding mechanisms

Humans have an impressive ability to discriminate between faces despite their similarity as visual patterns. This expertise relies on configural coding of spatial relations between face features and/or holistic coding of overall facial structure. These expert face-coding mechanisms appear to be engaged most effectively by upright faces, with inverted faces engaging primarily feature-coding mechanisms. We show that opposite figural aftereffects can be induced simultaneously for upright and inverted faces, demonstrating that distinct neural populations code upright and inverted faces. This result also suggests that expert (upright) face-coding mechanisms can be selectively adapted. These aftereffects occur for judgments of face normality and face gender and are robust to changes in face size, ruling out adaptation of low-level, retinotopically organized coding mechanisms. Our results suggest a resolution of a paradox in the face recognition literature. Neuroimaging studies have found surprisingly little orientation selectivity in the fusiform face area (FFA) despite evidence that this region plays a role in expert face coding and that expert face-coding mechanisms are selectively engaged by upright faces. Our results, demonstrating orientation-contingent adaptation of face-coding mechanisms, suggest that the FFA's apparent lack of orientation selectivity may be an artifact of averaging across distinct populations within the FFA that respond to upright and inverted faces.     

Distinct mechanisms mediate visual detection and identification

A core organizing principle for studies of the brain is that distinct neural pathways mediate distinct behavioral tasks [1, 2]. When two related tasks are mediated by a common pathway, studies of one are likely to generalize to the other. Here, we test whether performance on two laboratory tasks that model object detection and identification are mediated by common mechanisms of visual adaptation. Although both tasks rely on the luminance pattern in images, their demands on visual processing are quite different. Object detection requires discriminating image luminance differences associated with the light reflected from adjacent objects. To encode these differences reliably, neurons adapt their limited dynamic range to prevailing viewing conditions [3-6]. Object identification, on the other hand, demands a fixed response to light reflected from an object independent of illumination [7]. We compared performance in discrimination and identification tasks for simulated surfaces. In striking contrast to studies with less structured contexts, we found clear evidence that distinct processes mediate judgments in the two tasks. These results challenge models that account for perceived lightness entirely through the action of image-encoding mechanisms.     

Atypicalities in Perceptual Adaptation in Autism Do Not Extend to Perceptual Causality

A recent study showed that adaptation to causal events (collisions) in adults caused subsequent events to be less likely perceived as causal. In this study, we examined if a similar negative adaptation effect for perceptual causality occurs in children, both typically developing and with autism. Previous studies have reported diminished adaptation for face identity, facial configuration and gaze direction in children with autism. To test whether diminished adaptive coding extends beyond high-level social stimuli (such as faces) and could be a general property of autistic perception, we developed a child-friendly paradigm for adaptation of perceptual causality. We compared the performance of 22 children with autism with 22 typically developing children, individually matched on age and ability (IQ scores). We found significant and equally robust adaptation aftereffects for perceptual causality in both groups. There were also no differences between the two groups in their attention, as revealed by reaction times and accuracy in a change-detection task. These findings suggest that adaptation to perceptual causality in autism is largely similar to typical development and, further, that diminished adaptive coding might not be a general characteristic of autism at low levels of the perceptual hierarchy, constraining existing theories of adaptation in autism.     

Facial Trustworthiness Judgments in Children with ASD Are Modulated by Happy and Angry Emotional Cues

Appearance-based trustworthiness inferences may reflect the misinterpretation of emotional expression cues. Children and adults typically perceive faces that look happy to be relatively trustworthy and those that look angry to be relatively untrustworthy. Given reports of atypical expression perception in children with Autism Spectrum Disorder (ASD), the current study aimed to determine whether the modulation of trustworthiness judgments by emotional expression cues in children with ASD is also atypical. Cognitively-able children with and without ASD, aged 6–12 years, rated the trustworthiness of faces showing happy, angry and neutral expressions. Trust judgments in children with ASD were significantly modulated by overt happy and angry expressions, like those of typically-developing children. Furthermore, subtle emotion cues in neutral faces also influenced trust ratings of the children in both groups. These findings support a powerful influence of emotion cues on perceived trustworthiness, which even extends to children with social cognitive impairments.     

25OH维生素D水平检测与自闭症评定量表（CARS）评分的相关性及预测模型研究

摘要 目的：探究25OH维生素D（25(OH) D）水平检测与自闭症评定量表（CARS）评分的相关性及其评估自闭症严重程度的价值。方法：选取2020年4月~2022年3月在我院确诊的自闭症谱系障碍（ASD）患儿67例作为ASD组,并按照病情严重程度将所有患儿分为轻中度组46例,重度组36例。另募集来我科就诊无精神病史及家族史的健康查体儿童93例作为对照组。对比ASD组与对照组、ASD患儿轻中度组与重度组25(OH) D水平差异,分析ASD组患儿25(OH)D水平的影响因素,比较ASD组不同25(OH)D水平患儿CARS评分差异性,分析ASD患儿血清25(OH)D水平与CARS评分的相关性,并采用ROC曲线评估血清25(OH)D水平预估ASD严重程度的效能。结果：ASD组患儿血清25(OH) D水平显著低于于对照组（P<0.05）。相较于轻中度组,重度孤独症组患儿血清25(OH) D水平显著降低（P<0.05）。25(OH) D异常组患儿中母乳喂养、偏食及腹泻发生率显著高于25(OH) D正常组（P<0.05）。25(OH) D异常组患儿中CARS评分中的人际关系、模仿、情感反应、肢体动作、使用物体、对变化的适应、视觉反应、听觉反应及总分显著高于25(OH) D正常组（P<0.05）。CARS总分分与血清25(OH)D水平的成负相关性（r=-0.367,P=0.004）。血清25(OH)D水平预估ASD严重程度的AUC为0.716,敏感度为72.48%,特异度为78.65%。结论：血清25(OH)D在ASD患儿中成低表达,而且不同严重程度患儿血清25(OH)D差异表达,而且血清25(OH)D水平与CARS总分成负相关性,其作为评估ASD严重程度的生物标志物具有一定价值。     

Neural adjustments to chromatic blur

The perception of blur in images can be strongly affected by prior adaptation to blurry images or by spatial induction from blurred surrounds. These contextual effects may play a role in calibrating visual responses for the spatial structure of luminance variations in images. We asked whether similar adjustments might also calibrate the visual system for spatial variations in color. Observers adjusted the amplitude spectra of luminance or chromatic images until they appeared correctly focused, and repeated these measurements either before or after adaptation to blurred or sharpened images or in the presence of blurred or sharpened surrounds. Prior adaptation induced large and distinct changes in perceived focus for both luminance and chromatic patterns, suggesting that luminance and chromatic mechanisms are both able to adjust to changes in the level of blur. However, judgments of focus were more variable for color, and unlike luminance there was little effect of surrounding spatial context on perceived blur. In additional measurements we explored the effects of adaptation on threshold contrast sensitivity for luminance and color. Adaptation to filtered noise with a 1/f spectrum characteristic of natural images strongly and selectively elevated thresholds at low spatial frequencies for both luminance and color, thus transforming the chromatic contrast sensitivity function from lowpass to nearly bandpass. These threshold changes were found to reflect interactions between different spatial scales that bias sensitivity against the lowest spatial grain in the image, and may reflect adaptation to different stimulus attributes than the attributes underlying judgments of image focus. Our results suggest that spatial sensitivity for variations in color can be strongly shaped by adaptation to the spatial structure of the stimulus, but point to dissociations in these visual adjustments both between luminance and color and different measures of spatial sensitivity.     

Single-unit responses selective for whole faces in the human amygdala

The human amygdala is critical for social cognition from faces, as borne out by impairments in recognizing facial emotion following amygdala lesions [1] and differential activation of the amygdala by faces [2-5]. Single-unit recordings in the primate amygdala have documented responses selective for faces, their identity, or emotional expression [6, 7], yet how the amygdala represents face information remains unknown. Does it encode specific features of faces that are particularly critical for recognizing emotions (such as the eyes), or does it encode the whole face, a level of representation that might be the proximal substrate for subsequent social cognition? We investigated this question by recording from over 200 single neurons in the amygdalae of seven neurosurgical patients with implanted depth electrodes [8]. We found that approximately half of all neurons responded to faces or parts of faces. Approximately 20% of all neurons responded selectively only to the whole face. Although responding most to whole faces, these neurons paradoxically responded more when only a small part of the face was shown compared to when almost the entire face was shown. We suggest that the human amygdala plays a predominant role in representing global information about faces, possibly achieved through inhibition between individual facial features.     

A new approach to the diagnosis of deficits in processing faces: Potential application in autism research

Deficits in social communication are one of the behavioral signatures of autism spectrum disorder(ASD). Because faces are arguably the most important social stimuli that we encounter in everyday life, investigating the ability of individuals with ASD to process faces is thought to be important for understanding the nature of ASD. However, although a considerable body of evidence suggests that ASD individuals show specific impairments in face processing, a significant number of studies argue otherwise. Through a literature review, we found that this controversy is largely attributable to the different face tests used across different studies. Therefore, a more reliable and valid face test is needed. To this end, we performed a meta-analysis on data gleaned from a variety of face tests conducted on individuals with developmental prosopagnosia(DP) who suffer a selective deficit in face processing. Based on this meta-analysis, we selected an old/new face recognition test that relies on face memory as a standard diagnostic test for measuring specific face processing deficits. This test not only reliably reflects DP individuals' subjective experiences with faces in their daily lives, but also effectively differentiates deficits in face processing from deficits caused by other general problems. In addition, DP individuals' performance in this test predicts their performance in a variety of face tests that examine specific components of face processing(e.g., holistic processing of faces). Finally, this test can be easily administrated and is not overly sensitive to prior knowledge. In summary, this test can be used to evaluate face-processing ability, and it helped to resolve the controversy whether individuals with ASD exhibit face-processing deficits.