Bojana Kuzmanovic

Why we interact: On the functional role of the striatum in the subjective experience of social interaction

There is ample evidence that human primates strive for social contact and experience interactions with conspecifics as intrinsically rewarding. Focusing on gaze behavior as a crucial means of human interaction, this study employed a unique combination of neuroimaging, eye-tracking, and computer-animated virtual agents to assess the neural mechanisms underlying this component of behavior. In the interaction task, participants believed that during each interaction the agents gaze behavior could either be controlled by another participant or by a computer program. Their task was to indicate whether they experienced a given interaction as an interaction with another human participant or the computer program based on the agents reaction. Unbeknownst to them, the agent was always controlled by a computer to enable a systematic manipulation of gaze reactions by varying the degree to which the agent engaged in joint attention. This allowed creating a tool to distinguish neural activity underlying the subjective experience of being engaged in social and non-social interaction. In contrast to previous research, this allows measuring neural activity while participants experience active engagement in real-time social interactions. Results demonstrate that gaze-based interactions with a perceived human partner are associated with activity in the ventral striatum, a core component of reward-related neurocircuitry. In contrast, interactions with a computer-driven agent activate attention networks. Comparisons of neural activity during interaction with behaviorally naïve and explicitly cooperative partners demonstrate different temporal dynamics of the reward system and indicate that the mere experience of engagement in social interaction is sufficient to recruit this system.

Shall we do this together? Social gaze influences action control in a comparison group, but not in individuals with high-functioning autism:

Perceiving someone else’s gaze shift toward an object can influence how this object will be manipulated by the observer, suggesting a modulatory effect of a gaze-based social context on action control. High-functioning autism (HFA) is characterized by impairments of social interaction, which may be associated with an inability to automatically integrate socially relevant nonverbal cues when generating actions. To explore these hypotheses, we made use of a stimulus-response compatibility paradigm in which a comparison group and patients with HFA were asked to generate spatially congruent or incongruent motor responses to changes in a face, a face-like and an object stimulus. Results demonstrate that while in the comparison group being looked at by a virtual other leads to a reduction of reaction time costs associated with generating a spatially incongruent response, this effect is not present in the HFA group. We suggest that this modulatory effect of social gaze on action control might play an important role in direct social interactions by helping to coordinate one’s actions with those of someone else. Future research should focus on these implicit mechanisms of interpersonal alignment (‘online’ social cognition), which might be at the very heart of the difficulties individuals with autism experience in everyday social encounters.

The use of virtual characters to assess and train non-verbal communication in high-functioning autism.

High-functioning autism (HFA) is a neurodevelopmental disorder, which is characterized by life-long socio-communicative impairments on the one hand and preserved verbal and general learning and memory abilities on the other. One of the areas where particular difficulties are observable is the understanding of non-verbal communication cues. Thus, investigating the underlying psychological processes and neural mechanisms of non-verbal communication in HFA allows a better understanding of this disorder, and potentially enables the development of more efficient forms of psychotherapy and trainings. However, the research on non-verbal information processing in HFA faces several methodological challenges. The use of virtual characters (VCs) helps to overcome such challenges by enabling an ecologically valid experience of social presence, and by providing an experimental platform that can be systematically and fully controlled. To make this field of research accessible to a broader audience, we elaborate in the first part of the review the validity of using VCs in non-verbal behavior research on HFA, and we review current relevant paradigms and findings from social-cognitive neuroscience. In the second part, we argue for the use of VCs as either agents or avatars in the context of “transformed social interactions.” This allows for the implementation of real-time social interaction in virtual experimental settings, which represents a more sensitive measure of socio-communicative impairments in HFA. Finally, we argue that VCs and environments are a valuable assistive, educational and therapeutic tool for HFA.

Imaging first impressions: Distinct neural processing of verbal and nonverbal social information

First impressions profoundly influence our attitudes and behavior toward others. However, little is known about whether and to what degree the cognitive processes that underlie impression formation depend on the domain of the available information about the target person. To investigate the neural bases of the influence of verbal as compared to nonverbal information on interpersonal judgments, we identified brain regions where the BOLD signal parametrically increased with increasing strength of evaluation based on either short text vignettes or mimic and gestural behavior. While for verbal stimuli the increasing strength of subjective evaluation was correlated with increased neural activation of precuneus and posterior cingulate cortex (PC/PCC), a similar effect was observed for nonverbal stimuli in the amygdala. These findings support the assumption that qualitatively different cognitive operations underlie person evaluation depending upon the stimulus domain: while the processing of nonverbal person information may be more strongly associated with affective processing as indexed by recruitment of the amygdala, verbal person information engaged the PC/PCC that has been related to social inferential processing.

Neural correlates of "social gaze" processing in high-functioning autism under systematic variation of gaze duration.

Direct gaze is a salient nonverbal signal for social interest and the intention to communicate. In particular, the duration of anothers direct gaze can modulate our perception of the social meaning of gaze cues. However, both poor eye contact and deficits in social cognitive processing of gaze are specific diagnostic features of autism. Therefore, investigating neural mechanisms of gaze may provide key insights into the neural mechanisms related to autistic symptoms. Employing functional magnetic resonance imaging (fMRI) and a parametric design, we investigated the neural correlates of the influence of gaze direction and gaze duration on person perception in individuals with high-functioning autism (HFA) and a matched control group. For this purpose, dynamically animated faces of virtual characters, displaying averted or direct gaze of different durations (1 s, 2.5 s and 4 s) were evaluated on a four-point likeability scale. Behavioral results revealed that HFA participants showed no significant difference in likeability ratings depending on gaze duration, while the control group rated the virtual characters as increasingly likeable with increasing gaze duration. On the neural level, direct gaze and increasing direct gaze duration recruit regions of the social neural network (SNN) in control participants, indicating the processing of social salience and a perceived communicative intent. In participants with HFA however, regions of the social neural network were more engaged by averted and decreasing amounts of gaze, while the neural response for processing direct gaze in HFA was not suggestive of any social information processing.

Differential activation of memory-relevant brain regions during a dialysis cycle

Cognitive impairment is a common and largely undiagnosed finding in a significant number of dialysis patients. These alterations may result from concomitant cerebrovascular disease, hemodynamic instability, the uremic milieu, or changes induced by the dialysis process. In order to gain further insight into this, we recruited 12 stable chronic hemodialysis patients (without clinical neurological disease) and an age- and gender-matched cohort of 12 control individuals (without renal or neurological problems) in a prospective, single-center study. In order to disentangle the influence of dialysis itself on memory function, each dialysis patient was tested twice: once immediately before dialysis following a long weekend (t1) and again the day after this dialysis (t2). The control individuals were tested in the same time frame. Neuropsychological testing found that the control individuals performed significantly better in verbal learning, motor speed, task switching, verbal comprehension, word fluency, spatial visualization, spatial perception, and reasoning; all independent of the time point. Functional magnetic resonance imaging of the whole brain in seven hemodialysis patients found significantly more bilateral activation of the hippocampus during the verbal working memory task at t2 relative to t1 compared with their seven matched control counterparts. Thus, our study found differential and task-specific activation of memory-relevant brain areas during a dialysis cycle.

Dissociating animacy processing in high-functioning autism: Neural correlates of stimulus properties and subjective ratings

When movements indicate meaningful actions, even nonbiological objects induce the impression of “having a mind” or animacy. This basic social ability was investigated in adults with high-functioning autism (HFA, n = 13, and matched controls, n = 13) by systematically varying motion properties of simple geometric shapes. Critically, trial-by-trial variations of (1) motion complexity of stimuli, and of (2) participants’ individual animacy ratings were separately correlated with neural activity to dissociate cognitive strategies relying more closely on stimulus analysis vs. subjective experience. Increasing motion complexity did not yield any significant group differences, and in both groups, it correlated with neural activity in regions involved in perceptual and evaluative processing, including the ventral medial prefrontal cortex (mPFC), superior temporal gyrus (STG) and posterior cingulate cortex (PCC). In contrast, although there were no significant behavioral differences between the groups, increasing animacy ratings correlated with neural activity in the insula, STG, amygdala, dorsal mPFC and PCC more strongly in controls than in HFA. These results indicate that in HFA the evaluation of stimulus properties cuing for animacy is intact, while increasing subjective ratings do not seem to be robustly related to social processing, including spontaneous mental state inferences and experience of salience.

Neural correlates of reactive aggression in children with attention-deficit/hyperactivity disorder and comorbid disruptive behaviour disorders

Attention deficit hyperactivity disorder (ADHD) is often linked with impulsive and aggressive behaviour, indexed by high comorbidity rates between ADHD and disruptive behaviour disorders (DBD). The present study aimed to investigate underlying neural activity of reactive aggression in children with ADHD and comorbid DBD using functional neuroimaging techniques (fMRI).

Affective and motivational influences in person perception

Interpersonal impression formation is highly consequential for social interactions in private and public domains. These perceptions of others rely on different sources of information and processing mechanisms, all of which have been investigated in independent research fields. In social psychology, inferences about states and traits of others as well as activations of semantic categories and corresponding stereotypes have attracted great interest. On the other hand, research on emotion and reward demonstrated affective and motivational influences of social cues on the observer, which in turn modulate attention, categorization, evaluation, and decision processes. While inferential and categorical social processes have been shown to recruit a network of cortical brain regions associated with mentalizing and evaluation, the affective influence of social cues has been linked to subcortical areas that play a central role in detection of salient sensory input and reward processing. In order to extend existing integrative approaches to person perception, both the inferential-categorical processing of information about others, and affective and motivational influences of this information on the beholder should be taken into account.