Research Review: Social cognition and everyday social skills in children and adolescents with attention-deficit/hyperactivity disorder: a meta-analysis of case-control studies.

BACKGROUND: Previous studies that have assessed social cognition in Attention-Deficit/Hyperactivity Disorder (ADHD) have produced inconsistent findings. To summarize these data and shed light upon moderators that may explain observed inconsistencies, we conducted a systematic review and meta-analysis exploring social cognition (Theory of Mind (ToM), Empathy, Facial and Non-Facial Emotion Recognition) and Everyday Social Skills in children and adolescents with ADHD. METHODS: The current meta-analysis involved 142 studies including 652 effect sizes. These studies compared children and adolescents with ADHD (n = 8,300) and with typical development (n = 7,983). RESULTS: Participants with ADHD exhibited moderate to very large deficits in ToM (SMD = 0.84, 95% CI = 0.68-0.99), Facial Emotion Recognition (SMD = 0.63, 95% CI = 0.46-0.81), and Everyday Social Skills (SMD = 1.23, 95% CI = 1.08-1.37). The magnitude of these impairments was similar when considering effect sizes adjusted for some covariates and the methodological quality of the studies. Few studies have investigated Empathy and Non-Facial Emotion Recognition, which precludes definitive conclusions. CONCLUSIONS: Children and adolescents with ADHD experience robust impairments in ToM, Facial Emotion Recognition and Everyday Social Skills. Future studies should explore whether these deficits are a consequence of difficulties in other areas of cognition (e.g., executive functioning). We have made all our raw data open access to facilitate the use of the present work by the community (e.g., clinicians looking for tools, assessing social impairments, or researchers designing new studies).

Neural correlates of interoceptive accuracy: Beyond cardioception.

Interoceptive accuracy (IAc), the precision with which one assesses the signals arising from one's own body, is receiving increasing attention in the literature. IAc has mainly been approached as an individual trait and has been investigated through the cardiac modality using mostly non-ecological methods. Such studies consensually designate the anterior insular cortex as the main brain correlate of IAc. However, there is a lack of brain imaging studies investigating IAc in a broader and more ecological way. Here, we used a novel ecological task in which participants monitored their general bodily reactions to external events and investigated brain regions subtending intraindividual (i.e. trial-by-trial) variations of IAc. At each trial, participants had to rate the intensity of their bodily reactions to an emotional picture. We recorded participants' skin conductance response (SCR) to the picture as an indicator of actual physiological response intensity. We fitted a functional magnetic resonance imaging (fMRI) model using, as regressors, the SCR value, the rating and the product of the two (as a proxy of participants' IAc) obtained trial per trial. We observed that activity in the dorsomedial prefrontal cortex (dmPFC) increased when individuals' IAc decreased. This result reveals general mechanism of error processing in intraindividual variations of IAc, which are unspecific to interoception. Our result has a practical impact in the clinical domain. Namely, it supports the predictive coding framework whereby IAc deficits may reflect impairments in processing a mismatch between actual interoceptive signals and predictions.

Diagnosing gaze and arrow cueing effects in unilateral spatial neglect.

Individuals with left unilateral spatial neglect (USN) following a right hemisphere lesion show difficulty in orienting their attention toward stimuli presented on the left. In normal cognition, others' gaze direction and a pointing arrow naturally guide visual attention. Here, we explore a method to identify patients who may benefit from these skills as a base for compensation during rehabilitation. We tested gaze and arrow cueing effects in 26 healthy participants and in 13 patients with USN. Our data show that brain injuries causing USN do not affect gaze and arrow cueing in a consistent manner from one patient to another.

Minimal group membership biases early neural processing of emotional expressions.

Mere affiliation with a social group alters people's perception of other individuals. One suggested mechanism behind such influence is that group membership triggers divergent visual facial representations for in-group and out-group members, which could constrain face processing. Here, using electroencephalography (EEG) under functional magnetic resonance imagery (fMRI) during a group categorization task, we investigated the impact of mere affiliation to an arbitrary group on the processing of emotional faces. The results indicate that in- and out-group members trigger differential event-related potential activity, appearing 150 ms after presentation of group membership information, which correlated with medial prefrontal fMRI activity. Additionally, EEG activity in the earliest stages of face processing (30-100 ms after expression onset) dissociated unexpected group-related emotions (in-group anger and out-group joy) from expected ones and correlated with temporo-parietal junction fMRI activity. We discuss the possibility that such dissociation may result from top-down influences from divergent representations for in-group and out-group members. Taken together, the present results suggest that mere membership in an arbitrary group polarized expectations which constrain the first steps of face processing.

Watching Eyes effects: When others meet the self.

The perception of direct gaze-that is, of another individual's gaze directed at the observer-is known to influence a wide range of cognitive processes and behaviors. We present a new theoretical proposal to provide a unified account of these effects. We argue that direct gaze first captures the beholder's attention and then triggers self-referential processing, i.e., a heightened processing of stimuli in relation with the self. Self-referential processing modulates incoming information processing and leads to the Watching Eyes effects, which we classify into four main categories: the enhancement of self-awareness, memory effects, the activation of pro-social behavior, and positive appraisals of others. We advance that the belief to be the object of another's attention is embedded in direct gaze perception and gives direct gaze its self-referential power. Finally, we stress that the Watching Eyes effects reflect a positive impact on human cognition; therefore, they may have a therapeutic potential, which future research should delineate.

Selective attention effects on early integration of social signals: same timing, modulated neural sources.

Humans combine co-emitted social signals to predict other's immediate intentions and prepare an adapted response. However, little is known about whether attending to only one of co-emitted social signals impacts on its combination with other signals. Here, using electroencephalography, we address selective attention effects on early combination of social signals. We manipulated three visual cues: gaze direction, emotional expression, and pointing gesture, while participants performed either emotion or gaze direction judgments. Results showed that a temporal marker of social cues integration emerges 170ms after the stimulus onset, even if the integration of the three visual cues was not required to perform the task, as only one feature at a time was task relevant. Yet in addition to common temporal regions, the relative contribution of specific neural sources of this integration changed as a function of the attended feature: integration during emotion judgments was mainly implemented in classic limbic areas but in the dorsal pathway during gaze direction judgments. Together, these findings demonstrate that co-emitted social cues are integrated as long as they are relevant to the observer, even when they are irrelevant to the ongoing task.

Early binding of gaze, gesture, and emotion: neural time course and correlates.

Communicative intentions are transmitted by many perceptual cues, including gaze direction, body gesture, and facial expressions. However, little is known about how these visual social cues are integrated over time in the brain and, notably, whether this binding occurs in the emotional or the motor system. By coupling magnetic resonance and electroencephalography imaging in humans, we were able to show that, 200 ms after stimulus onset, the premotor cortex integrated gaze, gesture, and emotion displayed by a congener. At earlier stages, emotional content was processed independently in the amygdala (170 ms), whereas directional cues (gaze direction with pointing gesture) were combined at ∼190 ms in the parietal and supplementary motor cortices. These results demonstrate that the early binding of visual social signals displayed by an agent engaged the dorsal pathway and the premotor cortex, possibly to facilitate the preparation of an adaptive response to another person's immediate intention.

Social affordances: is the mirror neuron system involved?

We question the idea that the mirror neuron system is the substrate of social affordances perception, and we suggest that most of the activity seen in the parietal and premotor cortex of the human brain is independent of mirroring activity as characterized in macaques, but rather reflects a process of one's own action specification in response to social signals.

Look at me, I'll remember you: the perception of self-relevant social cues enhances memory and right hippocampal activity.

Being looked at by a person enhances the subsequent memorability of her/his identity. Here, we tested the specificity of this effect and its underlying brain processes. We manipulated three social cues displayed by an agent: Gaze Direction (Direct/Averted), Emotional Expression (Anger/Neutral), and Pointing gesture (Presence/Absence). Our behavioral experiment showed that direct as compared with averted gaze perception enhanced subsequent retrieval of face identity. Similar effect of enhanced retrieval was found when pointing finger was absent as compared with present but not for anger as compared with neutral expression. The fMRI results revealed amygdala activity for both Anger and Direct gaze conditions, suggesting emotional arousal. Yet, the right hippocampus, known to play a role in self-relevant memory processes, was only revealed during direct gaze perception. Further investigations suggest that right hippocampal activity was maximal for the most self-relevant social event (i.e. actor expressing anger and pointing toward the participant with direct gaze). Altogether, our results suggest that the perception of self-relevant social cues such as direct gaze automatically prompts "self-relevant memory" processes.

Measuring Gaze and Arrow Cuing Effects With a Short Test Adapted to Brain Damaged Patients With Unilateral Spatial Neglect: A Preliminary Study.

People with left unilateral spatial neglect (USN) following a right brain lesion show difficulty in orienting their attention toward stimuli presented on the left. However, cuing the stimuli with gaze direction or a pointing arrow can help some of them to compensate for this difficulty. In order to build a tool that helps to identify these patients, we needed a short version of the paradigm classically used to test gaze and arow cuing effects in healthy adults, adapted to the capacities of patients with severe attention deficit. Here, we tested the robustness of the cuing effects measured by such a short version in 48 young adult healthy participants, 46 older healthy participants, 10 patients with left USN following a right brain lesion (USN+), and 10 patients with right brain lesions but no USN (USN-). We observed gaze and arrow cuing effects in all populations, independently of age and presence or absence of a right brain lesion. In the neglect field, the USN+ group showed event greater cuing effect than older healthy participants and the USN- group. We showed that gaze and arrow cuing effects are powerful enough to be detected in a very short test adapted to the capacities of older patients with severe attention deficits, which increases their applicability in rehabilitation settings. We further concluded that our test is a suitable basis to develop a tool that will help neuropsychologists to identify USN patients who respond to gaze and/or arrow cuing in their neglect field.

Sensory Cueing of Autobiographical Memories in Normal Aging and Alzheimer's Disease: A Comparison Between Visual, Auditory, and Olfactory Information.

BACKGROUND: Alzheimer's disease (AD) is a chronic, neurodegenerative disease resulting in a progressive decline of autobiographical memories (AMs) which favors the development of psycho-behavioral disorders. One of the most popular psychosocial interventions in dementia care, Reminiscence Therapy, commonly uses sensory cueing to stimulate AMs retrieval. However, few empirical studies have investigated the impact of sensory stimulation on AMs retrieval in AD. OBJECTIVE: Our goal was to determine the most relevant cue for AMs retrieval in patients with early to mild AD when comparing odors, sounds and pictures. METHODS: Sixty AD patients, 60 healthy older adults (OA), and 60 healthy young adults (YA) participated in our study. Participants were presented with either 4 odors, 4 sounds, or 4 pictures. For each stimulus, they were asked to retrieve a personal memory, to rate it across 3 dimensions (emotionality, vividness, rarity) and then to date it. RESULTS: Overall, results showed no clear dominance of one sensory modality over the others in evoking higher-quality AMs. However, they show that using pictures is the better way to stimulate AD patients' AM, as it helps to retrieve a higher number of memories that are also less frequently retrieved, followed by odors. By contrast, auditory cueing with environmental sounds presented no true advantage. CONCLUSION: Our data should help dementia care professionals to increase the efficiency of Reminiscence Therapy using sensory elicitors. Other clinical implications and future directions are also discussed.

Investigating Eye Contact Effect on People's Name Retrieval in Normal Aging and in Alzheimer's Disease.

Difficulty in recalling people's name is one of the most universally experienced changes in old age and would also constitute one of the earliest symptom of Alzheimer's disease (AD). Direct gaze, i.e., another individual's gaze directed to the observer that leads to eye contact, has been shown to improve memory for faces and concomitant verbal information. Here, we investigated whether this effect extends to memory for Face-Name association and can thus enhance names' retrieval in normal aging and in AD, at the early stage of the disease. Twenty AD patients, 20 older adults and 25 young adults participated in our study. Subjects were presented with faces displaying either direct or averted gaze in association with a name presented orally. They were then asked to perform a surprise recognition test for each pair of stimuli, in a sequential fashion (i.e., first categorizing a face as old or new and then associating a name using a forced-choice procedure). Results showed that direct gaze does not improve memory for Face-Name association. Yet, we observed an overall direct gaze memory effect over faces and names independently, across our populations, showing that eye contact enhances the encoding of concomitantly presented stimuli. Our results are the first empirical evidence that eye contact benefits memory throughout the course of aging and lead to better delimit the actual power of eye contact on memory.

Social Contact Enhances Bodily Self-Awareness.

Human self-awareness is arguably the most important and revealing question of modern sciences. Converging theoretical perspectives link self-awareness and social abilities in human beings. In particular, mutual engagement during social interactions-or social contact-would boost self-awareness. Yet, empirical evidence for this effect is scarce. We recently showed that the perception of eye contact induces enhanced bodily self-awareness. Here, we aimed at extending these findings by testing the influence of social contact in auditory and tactile modalities, in order to demonstrate that social contact enhances bodily self-awareness irrespective of sensory modality. In a first experiment, participants were exposed to hearing their own first name (as compared to another unfamiliar name and noise). In a second experiment, human touch (as compared to brush touch and no-touch) was used as the social contact cue. In both experiments, participants demonstrated more accurate rating of their bodily reactions in response to emotional pictures following the social contact condition-a proxy of bodily self-awareness. Further analyses indicated that the effect of social contact was comparable across tactile, auditory and visual modalities. These results provide the first direct empirical evidence in support of the essential social nature of human self-awareness.

When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing.

Direct gaze or eye contact is a strong social signal, which triggers distinct processes as compared to other gaze directions. Thus, direct gaze could be early dissociated from averted gaze during the processing of gaze direction. In order to examine the processing of gaze contact relative to averted gaze, we studied evoked potentials in human adults in response to the apparent motion of gaze. Deviated and frontal faces were presented with a fixed gaze direction, followed by an apparent movement of the eyes either toward the subject or away from him/her. The results showed that the perception of direct relative to averted gaze evoked a greater, later and longer lasting N170, suggesting that gaze contact recruited more resources than averted gaze in the early stage of gaze direction processing. Furthermore, direct and averted motion of gaze elicited distinct ERP components between 160 and 210 ms, initiated over centro-parietal electrodes. Source reconstruction revealed the involvement of the Theory-of-Mind network, including the regions of the superior temporal sulcus, the medial prefrontal and the orbitofrontal cortices, in this early dissociation. In addition, the perception of gaze contact relative to averted gaze yielded increased fronto-central P3a and parieto-occipital P3b. All the results were significant whatever the head orientation. Our findings show that gaze contact, as compared to other gaze directions, is an essential social cue which recruits early specific processes. The dissociation between direct and averted gaze processing occurs as soon as 160 ms, involving the social brain network.

I know you can see me: Social attention influences bodily self-awareness.

It has recently been demonstrated that eye contact influences bodily self-awareness. Here, we investigated if the belief of being the target of another person's attention may also induce such influence. We created videos of an individual wearing two different pairs of sunglasses. We manipulated the participants to believe that they were in on-line connection with the individual and that one of the pairs of sunglasses was obstructed so that the individual could not see them through it. We demonstrated that the perception of an individual wearing see-through sunglasses, as compared to obstructed sunglasses or a low-level baseline condition, led to a greater correlation between the participants' rating of the intensity of their bodily reactions and their skin conductance response to emotional pictures. This shows that the belief to be watched by another social agent increases bodily self-awareness and further suggests that such belief is embedded in direct gaze perception.

Classification of autistic individuals and controls using cross-task characterization of fMRI activity.

Multivariate pattern analysis (MVPA) has been applied successfully to task-based and resting-based fMRI recordings to investigate which neural markers distinguish individuals with autistic spectrum disorders (ASD) from controls. While most studies have focused on brain connectivity during resting state episodes and regions of interest approaches (ROI), a wealth of task-based fMRI datasets have been acquired in these populations in the last decade. This calls for techniques that can leverage information not only from a single dataset, but from several existing datasets that might share some common features and biomarkers. We propose a fully data-driven (voxel-based) approach that we apply to two different fMRI experiments with social stimuli (faces and bodies). The method, based on Support Vector Machines (SVMs) and Recursive Feature Elimination (RFE), is first trained for each experiment independently and each output is then combined to obtain a final classification output. Second, this RFE output is used to determine which voxels are most often selected for classification to generate maps of significant discriminative activity. Finally, to further explore the clinical validity of the approach, we correlate phenotypic information with obtained classifier scores. The results reveal good classification accuracy (range between 69% and 92.3%). Moreover, we were able to identify discriminative activity patterns pertaining to the social brain without relying on a priori ROI definitions. Finally, social motivation was the only dimension which correlated with classifier scores, suggesting that it is the main dimension captured by the classifiers. Altogether, we believe that the present RFE method proves to be efficient and may help identifying relevant biomarkers by taking advantage of acquired task-based fMRI datasets in psychiatric populations.

Social influence on metacognitive evaluations: The power of nonverbal cues.

Metacognitive evaluations refer to the processes by which people assess their own cognitive operations with respect to their current goal. Little is known about whether this process is susceptible to social influence. Here we investigate whether nonverbal social signals spontaneously influence metacognitive evaluations. Participants performed a two-alternative forced-choice task, which was followed by a face randomly gazing towards or away from the response chosen by the participant. Participants then provided a metacognitive evaluation of their response by rating their confidence in their answer. In Experiment 1, the participants were told that the gaze direction was irrelevant to the task purpose and were advised to ignore it. The results revealed an effect of implicit social information on confidence ratings even though the gaze direction was random and therefore unreliable for task purposes. In addition, nonsocial cues (car) did not elicit this effect. In Experiment 2, the participants were led to believe that cue direction (face or car) reflected a previous participant's response to the same question-that is, the social information provided by the cue was made explicit, yet still objectively unreliable for the task. The results showed a similar social influence on confidence ratings, observed with both cues (car and face) but with an increased magnitude relative to Experiment 1. We additionally showed in Experiment 2 that social information impaired metacognitive accuracy. Together our results strongly suggest an involuntary susceptibility of metacognitive evaluations to nonverbal social information, even when it is implicit (Experiment 1) and unreliable (Experiments 1 and 2).

Source unreliability decreases but does not cancel the impact of social information on metacognitive evaluations.

Through metacognitive evaluations, individuals assess their own cognitive operations with respect to their current goals. We have previously shown that non-verbal social cues spontaneously influence these evaluations, even when the cues are unreliable. Here, we explore whether a belief about the reliability of the source can modulate this form of social impact. Participants performed a two-alternative forced choice task that varied in difficulty. The task was followed by a video of a person who was presented as being either competent or incompetent at performing the task. That person provided random feedback to the participant through facial expressions indicating agreement, disagreement or uncertainty. Participants then provided a metacognitive evaluation by rating their confidence in their answer. Results revealed that participants' confidence was higher following agreements. Interestingly, this effect was merely reduced but not canceled for the incompetent individual, even though participants were able to perceive the individual's incompetence. Moreover, perceived agreement induced zygomaticus activity, but only when the feedback was provided for difficult trials by the competent individual. This last result strongly suggests that people implicitly appraise the relevance of social feedback with respect to their current goal. Together, our findings suggest that people always integrate social agreement into their metacognitive evaluations, even when epistemic vigilance mechanisms alert them to the risk of being misinformed.

Social decisions affect neural activity to perceived dynamic gaze.

Gaze direction, a cue of both social and spatial attention, is known to modulate early neural responses to faces e.g. N170. However, findings in the literature have been inconsistent, likely reflecting differences in stimulus characteristics and task requirements. Here, we investigated the effect of task on neural responses to dynamic gaze changes: away and toward transitions (resulting or not in eye contact). Subjects performed, in random order, social (away/toward them) and non-social (left/right) judgment tasks on these stimuli. Overall, in the non-social task, results showed a larger N170 to gaze aversion than gaze motion toward the observer. In the social task, however, this difference was no longer present in the right hemisphere, likely reflecting an enhanced N170 to gaze motion toward the observer. Our behavioral and event-related potential data indicate that performing social judgments enhances saliency of gaze motion toward the observer, even those that did not result in gaze contact. These data and that of previous studies suggest two modes of processing visual information: a 'default mode' that may focus on spatial information; a 'socially aware mode' that might be activated when subjects are required to make social judgments. The exact mechanism that allows switching from one mode to the other remains to be clarified.

Eye contact elicits bodily self-awareness in human adults.

Eye contact is a typical human behaviour known to impact concurrent or subsequent cognitive processing. In particular, it has been suggested that eye contact induces self-awareness, though this has never been formally proven. Here, we show that the perception of a face with a direct gaze (that establishes eye contact), as compared to either a face with averted gaze or a mere fixation cross, led adult participants to rate more accurately the intensity of their physiological reactions induced by emotional pictures. Our data support the view that bodily self-awareness becomes more acute when one is subjected to another's gaze. Importantly, this effect was not related to a particular arousal state induced by eye contact perception. Rejecting the arousal hypothesis, we suggest that eye contact elicits a self-awareness process by enhancing self-focused attention in humans. We further discuss the implications of this proposal.