Social intuition: behavioral and neurobiological considerations.

Social intuition is instrumental in bringing about successful human interactions, yet its behavioral and neural underpinnings are still poorly understood. We focus in this article on the automatic, involuntary, nature of social intuition, rather than on higher-level cognitive and explicit Theory-of-Mind processes (which contribute to rendering social intuition meaningful in real-life situations). We argue that social-affective implicit learning plays a crucial role in establishing automatic social intuition. These implicit learning processes involve associations between the perception of other's bodily articulations, concurrent events, and the consequences or outcomes in terms of subsequent actions, affective valences and visceral states. The traditional non-social implicit learning paradigms do not allow one to draw conclusions about the role of implicit learning processes in social intuition, as they lack these vital characteristics typically associated with human actions. We introduce a new implicit learning paradigm, which aims to fill these gaps. It targets agile, rapid, social-affective learning processes, involving cue contingencies with a relatively simple structure, unlike the very complex structures that underpin the traditional tasks. The paradigm features matching social and non-social versions, allowing direct comparison. Preliminary data suggest equal performance of TD (typically-developed) and ASC (autism spectrum conditions) groups on the non-social version, but impaired implicit learning in ASC on the social version. We hypothesize that this reflects an anomalous use of implicitly learned affective information in ASC when judging other people. We further argue that the mirror neuron mechanism (MNM), which is part of the Action Observation Network, forms an integral part of the neural substrate for social intuition. In particular as there are indications that the MNM supports action anticipation, and that implicitly learned information can trigger MNM activation, which both seem vital to a social intuition ability. The insights that can be derived from comparing the performances of TD and ASC individuals on (non)social implicit learning tasks, and the implications for the role of MNM activation, are discussed.

Visual Attention to Dynamic Emotional Faces in Adults on the Autism Spectrum.

Using eye-tracking, we studied allocation of attention to faces where the emotional expression and eye-gaze dynamically changed in an ecologically-valid manner. We tested typically-developed (TD) adults low or high in autistic-like traits (Experiment 1), and adults with high-functioning autism (HFA; Experiment 2). All groups fixated more on the eyes than on any of the other facial area, regardless of emotion and gaze direction, though the HFA group fixated less on the eyes and more on the nose than TD controls. The sequence of dynamic facial changes affected the groups similarly, with reduced attention to the eyes and increased attention to the mouth. The results suggest that dynamic emotional face scanning patterns are stereotypical and differ only modestly between TD and HFA adults.

"Be careful what you recall": Retrieval-induced forgetting of genuine real-life autobiographical memories.

Which episodes from our lives will be remembered and which will be forgotten, and why? This question has still not been answered satisfactorily by research into autobiographical memory. Previous work has shown that retrieval-induced forgetting (RIF) might be a factor responsible for forgetting parts of the autobiographical memory content. However, none of the previous studies assessed RIF in memories for recent, controlled, personal events. We report here the results of an experiment in which autobiographical memories of real-life events were induced in a controlled, but fully naturalistic, manner under the disguise of team-building exercises, while an adapted RIF paradigm was applied to these memories. Results clearly showed the influence of RIF on autobiographical memory retrieval. These findings demonstrate conclusively that RIF occurs in everyday life when remembering personal events.

Sensorimotor representation of observed dyadic actions with varying agent involvement: an EEG mu study.

Observation of others' actions activates motor representations in sensorimotor cortex. Although action observation in the real-world often involves multiple agents displaying varying degrees of action involvement, most lab studies on action observation studied individual actions. We recorded EEG-mu suppression over sensorimotor cortex to investigate how the multi-agent nature of observed hand/arm actions is incorporated in sensorimotor action representations. Hereto we manipulated the extent of agent involvement in dyadic interactions presented in videos. In all clips two agents were present, of which agent-1 always performed the same action, while the involvement of agent-2 differed along three levels: (1) passive and uninvolved, (2) passively involved, (3) actively involved. Additionally, a no-action condition was presented. The occurrence of these four conditions was predictable thanks to cues at the start of each trial, which allowed to study possible mu anticipation effects. Dyadic interactions in which agent-2 was actively involved resulted in increased power suppression of the mu rhythm compared to dyadic interactions in which agent-2 was passively involved. The latter did not differ from actions in which agent-2 was present but not involved. No anticipation effects were found. The results suggest that the sensorimotor representation of a dyadic interaction takes into account the simultaneously performed bodily articulations of both agents, but no evidence was found for incorporation of their static articulated postures.

Could direct and generative retrieval be two flips of the same coin? A dual-task paradigm study.

Autobiographical memories are thought to be retrieved using two possible ways: a generative one, which is effortful and follows a general-to-specific pathway, and a direct one, which is automatic and relatively effortless. These two retrieve processes are known to differ on the quantitative side (especially considering retrieval times), from a qualitative point of view; however, evidence is missing. Here, we aimed to disentangle this question by taking advantage of a dual-task paradigm in which the different tasks tax different executive functions. Participants were asked to perform an autobiographical memory task under three different conditions: no cognitive load, non-visual cognitive load and visual cognitive load. On the quantitative side, results replicated previous findings with generative processes being slower compared with direct ones. Conversely, on the qualitative side, results indicated that the retrieval times of both direct and generative retrieval processes varied similarly according to the dual-task condition, thus supporting the idea that the same memory process could underlie both retrievals.

Sensorimotor anticipation of others' actions in real-world and video settings: Modulation by level of engagement?

Electroencephalography (EEG) studies investigating social cognition have used both video and real-world stimuli, often without a strong reasoning as to why one or the other was chosen. Video stimuli can be selected for practical reasons, while naturalistic real-world stimuli are ecologically valid. The current study investigated modulatory effects on EEG mu (8-13 Hz) suppression, directly prior to the onset - and during the course - of observed actions, related to real-world and video settings. Recordings were made over sensorimotor cortex and stimuli in both settings consisted of identical (un)predictable object-related grasping and placing actions. In both settings, a very similar mu suppression was found during unfolding of the action, irrespective of predictability. However, mu suppression related to the anticipation of upcoming predictable actions was found exclusively in the real-world setting. Thus, even though the presentation setting does not seem to modulate mu suppression during action observation, it does affect the anticipation-related mu suppression. We discuss the possibility that this may be due to increased social engagement in real-world settings, which in particular affects anticipation. The findings emphasize the importance of using real-world stimuli to bring out the subtle, anticipatory, aspects related to action observation.

Memory for facial expressions on the autism spectrum: The influence of gaze direction and type of expression.

Face memory research in autism has largely neglected memory for facial expressions, in favor of memory for identity. This study in three experiments examined the role of gaze direction and type of expression on memory for facial expressions in relation to the autism spectrum. In the learning phase, four combinations of facial expressions (joy/anger) and gaze direction (toward/away), displayed by 16 different identities, were presented. In a subsequent surprise test the same identities were presented displaying neutral expressions, and the expression of each identity had to be recalled. In Experiment 1, typically-developed (TD) individuals with low and high Autism Quotient (AQ) scores were tested with three repetitions of each emotion/gaze combination, which did not produce any modulations. In Experiment 2, another group of TD individuals with low and high AQ scores were tested with eight repetitions, resulting in a "happy advantage" and a "direct gaze advantage", but no interactions. In Experiment 3, individuals with high-functioning autism (HFA) and a matched TD group were tested using eight repetitions. The HFA group revealed no emotion or gaze effects, while the matched TD group showed both a happy and a direct gaze advantage, and again no interaction. The results suggest that in autistic individuals the memory for facial expressions is intact, but is not modulated by the person's expression type and gaze direction. We discuss whether anomalous implicit learning of facial cues could have contributed to these findings, its relevance for social intuition, and its possible contribution to social deficits in autism. LAY SUMMARY: It has often been found that memory for someone's face (facial identity) is less good in autism. However, it is not yet known whether memory for someone's facial expression is also less good in autism. In this study, the memory for expressions of joy and anger was investigated in typically-developed (TD) individuals who possessed either few or many autistic-like traits (Experiments 1 and 2), and in individuals with high-functioning autism (Experiment 3). The gaze direction was also varied (directed either toward, or away from, the observer). We found that TD individuals best remembered expressions of joy, and remembered expressions of both joy and anger better when the gaze was directed at them. These effects did not depend on the extent to which they possessed autistic-like traits. Autistic participants remembered the facial expression of a previously encountered person as good as TD participants did. However, in contrast to the TD participants, the memory of autistic participants was not influenced by the expression type and gaze direction of the previously encountered persons. We discuss whether this may lead to difficulties in the development of social intuition, which in turn could give rise to difficulties in social interaction that are characteristic for autism.

Are adaptation aftereffects for facial emotional expressions affected by prior knowledge about the emotion?

Accurate perception of the emotional signals conveyed by others is crucial for successful social interaction. Such perception is influenced not only by sensory input, but also by knowledge we have about the others' emotions. This study addresses the issue of whether knowing that the other's emotional state is congruent or incongruent with their displayed emotional expression ("genuine" and "fake", respectively) affects the neural mechanisms underpinning the perception of their facial emotional expressions. We used a visual adaptation paradigm to investigate this question in three experiments employing increasing adaptation durations. The adapting stimuli consisted of photographs of emotional facial expressions of joy and anger, purported to reflect (in-)congruency between felt and expressed emotion, displayed by professional actors. A Validity checking procedure ensured participants had the correct knowledge about the (in-)congruency. Significantly smaller adaptation aftereffects were obtained when participants knew that the displayed expression was incongruent with the felt emotion, following all tested adaptation periods. This study shows that knowledge relating to the congruency between felt and expressed emotion modulates face expression aftereffects. We argue that this reflects that the neural substrate responsible for the perception of facial expressions of emotion incorporates the presumed felt emotion underpinning the expression.

Sensorimotor cortex activation during anticipation of upcoming predictable but not unpredictable actions.

The mirror neuron system (MNS) becomes active during action execution and action observation, which is presumably reflected by reductions in mu (8-13 Hz) activity in the electroencephalogram over the sensorimotor cortex. The function of the MNS is still fiercely debated. The current study aimed to investigate a role of the MNS in anticipating others' actions by examining whether the MNS was activated - indexed by mu power suppression - prior to the onset of observed actions when the onset and type of action could be predicted on the basis of environmental cues. Young adults performed and observed cued grasping and placing actions in a card game in a real-life setting, while the predictability of the observed actions was manipulated using rules. Significant mu suppression, relative to within-trial baseline activity, was found both prior to and during executed actions, but also during action observation, and, crucially, prior to observed actions provided they were predictable. No anticipatory mu reductions were found prior to unpredictable observed actions. These results suggest top-down modulation of MNS activity by conceptual knowledge. This is the first study to demonstrate mu suppression prior to action onset - possibly reflecting MNS anticipatory activity - by explicitly manipulating predictability.

The Role of Pattern Extrapolation in the Perception of Dynamic Facial Expressions in Autism Spectrum Disorder.

Changes in the intensity and type of facial expressions reflect alterations in the emotional state of the agent. Such "direct" access to the other's affective state might, top-down, influence the perception of the facial expressions that gave rise to the affective state inference. Previously, we described a perceptual bias occurring when the last, neutral, expression of offsets of facial expressions (joy-to-neutral and anger-to-neutral), was evaluated. Individuals with high-functioning autism (HFA) and matched typically developed (TD) individuals rated the neutral expression at the end of the joy-offset videos as slightly angry and the identical neutral expression at the end of the anger-offset videos as slightly happy ("overshoot" bias). That study suggested that the perceptual overshoot response bias in the TD group could be best explained by top-down "emotional anticipation," i.e., the involuntary/automatic anticipation of the agent's next emotional state of mind, generated by the immediately preceding perceptual history (low-level mind reading). The experimental manipulations further indicated that in the HFA group the "overshoot" was better explained by contrast effects between the first and last facial expressions, both presented for a relatively long period of 400 ms. However, in principle, there is another, more parsimonious, explanation, which is pattern extrapolation or representational momentum (RM): the extrapolation of a pattern present in the dynamic sequence. This hypothesis is tested in the current study, in which 18 individuals with HFA and a matched control group took part. In a base-line condition, joy-offset and anger-offset video-clips were presented. In the new experimental condition, the clips were modified so as to create an offset-onset-offset pattern within each sequence (joy-to-anger-to-neutral and anger-to-joy-to-neutral). The final neutral expressions had to be evaluated. The overshoot bias was confirmed in the base-line condition for both TD and HFA groups, while the experimental manipulation removed the bias in both groups. This outcome ruled out pattern extrapolation or RM as explanation for the perceptual "overshoot" bias in the HFA group and suggested a role for facial contrast effects in HFA. This is compatible with the view that ASD individuals tend to lack the spontaneous "tracking" of changes in the others' affective state and hence show no or reduced emotional anticipation.

Action adaptation during natural unfolding social scenes influences action recognition and inferences made about actor beliefs.

When observing another individual's actions, we can both recognize their actions and infer their beliefs concerning the physical and social environment. The extent to which visual adaptation influences action recognition and conceptually later stages of processing involved in deriving the belief state of the actor remains unknown. To explore this we used virtual reality (life-size photorealistic actors presented in stereoscopic three dimensions) to see how visual adaptation influences the perception of individuals in naturally unfolding social scenes at increasingly higher levels of action understanding. We presented scenes in which one actor picked up boxes (of varying number and weight), after which a second actor picked up a single box. Adaptation to the first actor's behavior systematically changed perception of the second actor. Aftereffects increased with the duration of the first actor's behavior, declined exponentially over time, and were independent of view direction. Inferences about the second actor's expectation of box weight were also distorted by adaptation to the first actor. Distortions in action recognition and actor expectations did not, however, extend across different actions, indicating that adaptation is not acting at an action-independent abstract level but rather at an action-dependent level. We conclude that although adaptation influences more complex inferences about belief states of individuals, this is likely to be a result of adaptation at an earlier action recognition stage rather than adaptation operating at a higher, more abstract level in mentalizing or simulation systems.

Emotional Actions Are Coded via Two Mechanisms: With and without Identity Representation.

Accurate perception of an individual's identity and emotion derived from their actions and behavior is essential for successful social functioning. Here we determined the role of identity in the representation of emotional whole-body actions using visual adaptation paradigms. Participants adapted to actors performing different whole-body actions in a happy and sad fashion. Following adaptation subsequent neutral actions appeared to convey the opposite emotion. We demonstrate two different emotional action aftereffects showing distinctive adaptation characteristics. For one short-lived aftereffect, adaptation to the emotion expressed by an individual resulted in biases in the perception of the expression of emotion by other individuals, indicating an identity-independent representation of emotional actions. A second, longer lasting, aftereffect was observed where adaptation to the emotion expressed by an individual resulted in longer-term biases in the perception of the expressions of emotion only by the same individual; this indicated an additional identity-dependent representation of emotional actions. Together, the presence of these two aftereffects indicates the existence of two mechanisms for coding emotional actions, only one of which takes into account the actor's identity. The results that we observe might parallel processing of emotion from face and voice.

Atypical emotional anticipation in high-functioning autism.

BACKGROUND: Understanding and anticipating others' mental or emotional states relies on the processing of social cues, such as dynamic facial expressions. Individuals with high-functioning autism (HFA) may process these cues differently from individuals with typical development (TD) and purportedly use a 'mechanistic' rather than a 'mentalistic' approach, involving rule- and contingency-based interpretations of the stimuli. The study primarily aimed at examining whether the judgments of facial expressions made by individuals with TD and HFA would be similarly affected by the immediately preceding dynamic perceptual history of that face. A second aim was to explore possible differences in the mechanisms underpinning the perceptual judgments in the two groups. METHODS: Twenty-two adults with HFA and with TD, matched for age, gender and IQ, were tested in three experiments in which dynamic, 'ecologically valid' offsets of happy and angry facial expressions were presented. Participants evaluated the expression depicted in the last frame of the video clip by using a 5-point scale ranging from slightly angry via neutral to slightly happy. Specific experimental manipulations prior to the final facial expression of the video clip allowed examining contributions of bottom-up mechanisms (sequential contrast/context effects and representational momentum) and a top-down mechanism (emotional anticipation) to distortions in the perception of the final expression. RESULTS: In experiment 1, the two groups showed a very similar perceptual bias for the final expression of joy-to-neutral and anger-to-neutral videos (overshoot bias). In experiment 2, a change in the actor's identity during the clip removed the bias in the TD group, but not in the HFA group. In experiment 3, neutral-to-joy/anger-to-neutral sequences generated an undershoot bias (opposite to the overshoot) in the TD group, whereas no bias was observed in the HFA group. CONCLUSIONS: We argue that in TD individuals the perceptual judgments of other's facial expressions were underpinned by an automatic emotional anticipation mechanism. In contrast, HFA individuals were primarily influenced by visual features, most notably the contrast between the start and end expressions, or pattern extrapolation. We critically discuss the proposition that automatic emotional anticipation may be induced by motor simulation of the perceived dynamic facial expressions and discuss its implications for autism.

Impaired identification of impoverished animate but not inanimate objects in adults with high-functioning autism spectrum disorder.

The ability to identify animate and inanimate objects from impoverished images was investigated in adults with high-functioning autism spectrum disorder (HFA) and in matched typically developed (TD) adults, using a newly developed task. Consecutive frames were presented containing Gabor elements that slightly changed orientation from one frame to the next. For a subset of elements, the changes were such that these elements gradually formed the outline of an object. Elements enclosed within the object's outline gradually adopted one and the same orientation, outside elements adopted random orientations. The subjective experience was that of an object appearing out of a fog. The HFA group required significantly more frames to identify the impoverished objects than the TD group. Crucially, this difference depended on the nature of the objects: the HFA group required significantly more frames to identify animate objects, but with respect to the identification of inanimate objects the groups did not differ. The groups also did not differ with respect to the number and type of incorrect guesses they made. The results suggest a specific impairment in individuals with HFA in identifying animate objects. A number of possible explanations are discussed.

Involuntary social cue integration in patients with obsessive compulsive disorder.

OBJECTIVE: Patients with obsessive compulsive disorder (OCD) have inferior social functioning compared to healthy controls, but the exact nature of these social deficits, and the underpinning mechanisms, are unknown. We sought to investigate social functioning in patients with OCD by measuring their involuntary/spontaneous processing of social cues using a specifically designed test, which might reveal deficits in these patients that explicit voluntary tasks do not detect. METHODS: The sample of the study consisted of an OCD group (n = 25) and a control group (n = 26). Both groups performed an adaptation of the Social Distance Judgment Task (SDJT; Jellema et al., 2009), in which participants have to judge the geometrical distance between two human cartoon figures presented on a computer screen. Head/gaze direction and body direction were manipulated to be either compatible, i.e. both directed to the left or to the right (Compatible condition) or incompatible, i.e. body directed toward the observer (frontal view) and head/gaze directed to the left or right (Incompatible condition). RESULTS: In the Compatible condition, controls nor OCD patients were influenced by the social cues in their judgments of the geometrical distances. However, in the Incompatible condition, where the attentional cue was more conspicuous, both groups were influenced by the cues, but the controls to a significantly larger extent than the OCD patients. CONCLUSIONS: This study showed that patients with OCD are less likely, compared to controls, to automatically/spontaneously integrate the other's direction of attention into their visual percept. This may have resulted in their judgments of the geometrical distances between the agents to be more accurate than those of controls. The suggested impairment in automatically integrating social cues may have important repercussions for the social functioning of OCD patients.

Beyond face value: does involuntary emotional anticipation shape the perception of dynamic facial expressions?

Emotional facial expressions are immediate indicators of the affective dispositions of others. Recently it has been shown that early stages of social perception can already be influenced by (implicit) attributions made by the observer about the agent's mental state and intentions. In the current study possible mechanisms underpinning distortions in the perception of dynamic, ecologically-valid, facial expressions were explored. In four experiments we examined to what extent basic perceptual processes such as contrast/context effects, adaptation and representational momentum underpinned the perceptual distortions, and to what extent 'emotional anticipation', i.e. the involuntary anticipation of the other's emotional state of mind on the basis of the immediate perceptual history, might have played a role. Neutral facial expressions displayed at the end of short video-clips, in which an initial facial expression of joy or anger gradually morphed into a neutral expression, were misjudged as being slightly angry or slightly happy, respectively (Experiment 1). This response bias disappeared when the actor's identity changed in the final neutral expression (Experiment 2). Videos depicting neutral-to-joy-to-neutral and neutral-to-anger-to-neutral sequences again produced biases but in opposite direction (Experiment 3). The bias survived insertion of a 400 ms blank (Experiment 4). These results suggested that the perceptual distortions were not caused by any of the low-level perceptual mechanisms (adaptation, representational momentum and contrast effects). We speculate that especially when presented with dynamic, facial expressions, perceptual distortions occur that reflect 'emotional anticipation' (a low-level mindreading mechanism), which overrules low-level visual mechanisms. Underpinning neural mechanisms are discussed in relation to the current debate on action and emotion understanding.

(Re-)conceptualisation in Asperger's syndrome and typical individuals with varying degrees of autistic-like traits.

The abilities to form new concepts from scratch (conceptualisation), and to flexibly switch from one concept to another (re-conceptualisation), were investigated in adults with Asperger's Syndrome and in typically-developed adults with low and high autism spectrum quotients. In consecutively presented morphs, containing increasing percentages of animate or inanimate objects, the emerging objects had to be identified. The abilities to conceptualise and reconceptualise became increasingly impaired with increasing autistic(-like) traits. Across both tasks, all groups recognised animate objects quicker than inanimate objects. However, this 'animate advantage' was differently affected by the two tasks. In the Reconceptualisation task, the 'animate advantage' gradually disappeared with increasing autistic(-like) traits, whereas in the Conceptualisation task it remained present.

Linguistic alignment in adults with and without Asperger's syndrome.

Individuals with Asperger's syndrome (AS) often have difficulties with social interactions and conversations. We investigated if these difficulties could be attributable to a deficit in the ability to linguistically converge with an interlocutor, which is posited to be important for successful communication. To that end, participants completed two cooperative tasks with a confederate, which allowed us to measure linguistic alignment with the confederate in terms of lexical choice, syntactic structure and spatial frame of reference. There was no difference in the performance of individuals with AS and matched controls and both groups showed significant alignment with the confederate at all three levels. We conclude that linguistic alignment is intact in adults with AS engaged in structured, goal-directed social interactions.

Implicit social learning in relation to autistic-like traits.

We investigated if variation in autistic traits in the typically-developed population (using the Autism-spectrum Quotient, AQ) influenced implicit learning of social information. In the learning phase, participants repeatedly observed two identities whose gaze and expression conveyed either a pro- or antisocial disposition. These identities were then employed in a gaze-cueing paradigm. Participants made speeded responses to a peripheral target that was spatially pre-cued by a non-predictive gaze direction. The low AQ group (n = 50) showed a smaller gaze-cueing effect for the antisocial than for the prosocial identity. The high AQ group (n = 48) showed equivalent gaze-cueing for both identities. Others' intentions/dispositions can be learned implicitly and affect subsequent responses to their behavior. This ability is impaired with increasing levels of autistic traits.