The neural and computational systems of social learning.

Learning the value of stimuli and actions from others - social learning - adaptively contributes to individual survival and plays a key role in cultural evolution. We review research across species targeting the neural and computational systems of social learning in both the aversive and appetitive domains. Social learning generally follows the same principles as self-experienced value-based learning, including computations of prediction errors and is implemented in brain circuits activated across task domains together with regions processing social information. We integrate neural and computational perspectives of social learning with an understanding of behaviour of varying complexity, from basic threat avoidance to complex social learning strategies and cultural phenomena.

How emotional contexts modulate item memory in individuals with high and low negative affect and worry.

Emotional stimuli are usually remembered with high confidence. Yet, it remains unknown whether-in addition to memory for the emotional stimulus itself-memory for a neutral stimulus encountered just after an emotional one can be enhanced. Further, little is known about the interplay between emotion elicited by a stimulus and emotion relating to affective dispositions. To address these questions, we examined (1) how emotional valence and arousal of a context image preceding a neutral item image affect memory of the item, and (2) how such memory modulation is affected by two hallmark features of emotional disorders: trait negative affect and tendency to worry. In two experiments, participants encoded a series of trials in which an emotional (negative, neutral, or positive) context image was followed by a neutral item image. In experiment 1 (n = 42), items presented seconds after negative context images were remembered better and with greater confidence compared to those presented after neutral and positive ones. Arousal ratings of negative context images were higher compared to neutral and positive ones and the likelihood of correctly recognizing an item image was related to higher arousal of the context image. In experiment 2 (n = 59), better item memory was related to lower trait negative affect. Participants with lower trait negative affect or tendency to worry displayed higher confidence compared to those with high negative affect or tendency to worry. Our findings describe an emotional "carry-over" effect elicited by a context image that enhances subsequent item memory on a trial-by-trial basis, however, not in individuals with high trait negative affect who seem to have a general memory disadvantage.

Observation of others' threat reactions recovers memories previously shaped by firsthand experiences.

Information about dangers can spread effectively by observation of others' threat responses. Yet, it is unclear if such observational threat information interacts with associative memories that are shaped by the individual's direct, firsthand experiences. Here, we show in humans and rats that the mere observation of a conspecific's threat reactions reinstates previously learned and extinguished threat responses in the observer. In two experiments, human participants displayed elevated physiological responses to threat-conditioned cues after observational reinstatement in a context-specific manner. The elevation of physiological responses (arousal) was further specific to the context that was observed as dangerous. An analogous experiment in rats provided converging results by demonstrating reinstatement of defensive behavior after observing another rat's threat reactions. Taken together, our findings provide cross-species evidence that observation of others' threat reactions can recover associations previously shaped by direct, firsthand aversive experiences. Our study offers a perspective on how retrieval of threat memories draws from associative mechanisms that might underlie both observations of others' and firsthand experiences.

Learning about threat from friends and strangers is equally effective: An fMRI study on observational fear conditioning.

Humans often benefit from social cues when learning about the world. For instance, learning about threats from others can save the individual from dangerous first-hand experiences. Familiarity is believed to increase the effectiveness of social learning, but it is not clear whether it plays a role in learning about threats. Using functional magnetic resonance imaging, we undertook a naturalistic approach and investigated whether there was a difference between observational fear learning from friends and strangers. Participants (observers) witnessed either their friends or strangers (demonstrators) receiving aversive (shock) stimuli paired with colored squares (observational learning stage). Subsequently, participants watched the same squares, but without receiving any shocks (direct-expression stage). We observed a similar pattern of brain activity in both groups of observers. Regions related to threat responses (amygdala, anterior insula, anterior cingulate cortex) and social perception (fusiform gyrus, posterior superior temporal sulcus) were activated during the observational phase, possibly reflecting the emotional contagion process. The anterior insula and anterior cingulate cortex were also activated during the subsequent stage, indicating the expression of learned threat. Because there were no differences between participants observing friends and strangers, we argue that social threat learning is independent of the level of familiarity with the demonstrator.

Does gender matter? The association between different digital media activities and adolescent well-being.

BACKGROUND: Previous research on the relationship between social media use and well-being in adolescents has yielded inconsistent results. We addressed this issue by examining the association between various digital media activities, including a new and differentiated measure of social media use, and well-being (internalizing symptoms) in adolescent boys and girls. METHOD: The sample was drawn from the four cross-sectional surveys from the Öckerö project (2016-2019) in eight municipalities in southern Sweden, consisting of 3957 adolescents in year 7 of compulsory education, aged 12-13. We measured the following digital media activities: playing games and three different activities of social media use (chatting, online sociability, and self-presentation). Our outcome measure was internalizing symptoms. Hypotheses were tested with linear regression analysis. RESULTS: Social media use and playing games were positively associated with internalizing symptoms. The effect of social media use was conditional on gender, indicating that social media use was only associated with internalizing symptoms for girls. Of the social media activities, only chatting and self-presentation (posting information about themselves) were positively associated with internalizing symptoms. Self-presentation was associated with internalizing symptoms only for girls. CONCLUSION: Our study shows the importance of research going beyond studying the time spent on social media to examine how different kinds of social media activities are associated with well-being. Consistent with research in psychology, our results suggest that young girls posting information about themselves (i.e. self-presentation) might be especially vulnerable to display internalizing symptoms.

Social threat learning transfers to decision making in humans.

In today's world, mass-media and online social networks present us with unprecedented exposure to second-hand, vicarious experiences and thereby the chance of forming associations between previously innocuous events (e.g., being in a subway station) and aversive outcomes (e.g., footage or verbal reports from a violent terrorist attack) without direct experience. Such social threat, or fear, learning can have dramatic consequences, as manifested in acute stress symptoms and maladaptive fears. However, most research has so far focused on socially acquired threat responses that are expressed as increased arousal rather than active behavior. In three experiments (n = 120), we examined the effect of indirect experiences on behaviors by establishing a link between social threat learning and instrumental decision making. We contrasted learning from direct experience (i.e., Pavlovian conditioning) (experiment 1) against two common forms of social threat learning-social observation (experiment 2) and verbal instruction (experiment 3)-and how this learning transferred to subsequent instrumental decision making using behavioral experiments and computational modeling. We found that both types of social threat learning transfer to decision making in a strong and surprisingly inflexible manner. Notably, computational modeling indicated that the transfer of observational and instructed threat learning involved different computational mechanisms. Our results demonstrate the strong influence of others' expressions of fear on one's own decisions and have important implications for understanding both healthy and pathological human behaviors resulting from the indirect exposure to threatening events.

Integration of social cues and individual experiences during instrumental avoidance learning.

Learning to avoid harmful consequences can be a costly trial-and-error process. In such situations, social information can be leveraged to improve individual learning outcomes. Here, we investigated how participants used their own experiences and others' social cues to avoid harm. Participants made repeated choices between harmful and safe options, each with different probabilities of generating shocks, while also seeing the image of a social partner. Some partners made predictive gaze cues towards the harmful choice option while others cued an option at random, and did so using neutral or fearful facial expressions. We tested how learned social information about partner reliability transferred across contexts by letting participants encounter the same partner in multiple trial blocks while facing novel choice options. Participants' decisions were best explained by a reinforcement learning model that independently learned the probabilities of options being safe and of partners being reliable and combined these combined these estimates to generate choices. Advice from partners making a fearful facial expression influenced participants' decisions more than advice from partners with neutral expressions. Our results showed that participants made better decisions when facing predictive partners and that they cached and transferred partner reliability estimates into new blocks. Using simulations we show that participants' transfer of social information into novel contexts is better adapted to variable social environments where social partners may change their cuing strategy or become untrustworthy. Finally, we found no relation between autism questionnaire scores and performance in our task, but do find autism trait related differences in learning rate parameters.

Neural Pattern Similarity Unveils the Integration of Social Information and Aversive Learning.

Attributing intentions to others' actions is important for learning to avoid their potentially harmful consequences. Here, we used functional magnetic resonance imaging multivariate pattern analysis to investigate how the brain integrates information about others' intentions with the aversive outcome of their actions. In an interactive aversive learning task, participants (n = 33) were scanned while watching two alleged coparticipants (confederates)-one making choices intentionally and the other unintentionally-leading to aversive (a mild shock) or safe (no shock) outcomes to the participant. We assessed the trial-by-trial changes in participants' neural activation patterns related to observing the coparticipants and experiencing the outcome of their choices. Participants reported a higher number of shocks, more discomfort, and more anger to shocks given by the intentional player. Intentionality enhanced responses to aversive actions in the insula, anterior cingulate cortex, inferior frontal gyrus, dorsal medial prefrontal cortex, and the anterior superior temporal sulcus. Our findings indicate that neural pattern similarities index the integration of social and threat information across the cortex.

Physiological synchrony predicts observational threat learning in humans.

Understanding how information about threats in the environment is shared and transmitted between individuals is crucial for explaining adaptive, survival-related behaviour in humans and other animals, and for developing treatments for phobias and other anxiety disorders. Research across species has shown that observing a conspecific's, a 'demonstrator's,' threat responses causes strong and persistent threat memories in the 'observer'. Here, we examined if physiological synchrony between demonstrator and observer can serve to predict the strength of observationally acquired conditioned responses. We measured synchrony between demonstrators' and observers' phasic electrodermal signals during learning, which directly reflects autonomic nervous system activity. Prior interpersonal synchrony predicted the strength of the observer's later skin conductance responses to threat predicting stimuli, in the absence of the demonstrator. Dynamic coupling between an observer's and a demonstrator's autonomic nervous system activity may reflect experience sharing processes facilitating the formation of observational threat associations.

Help or flight? Increased threat imminence promotes defensive helping in humans.

In humans and other mammals, defensive responses to danger vary with threat imminence, but it is unknown how those responses affect decisions to help conspecifics. Here, we manipulated threat imminence to investigate the impact of different defensive states on human helping behaviour. Ninety-eight healthy adult participants made trial-by-trial decisions about whether to help a co-participant avoid an aversive shock, at the risk of receiving a shock themselves. Helping decisions were prompted under imminent or distal threat, based on temporal distance to the moment of shock administration to the co-participant. Results showed that, regardless of how likely participants were to also receive a shock, they helped the co-participant more under imminent than distal threat. Reaction times and cardiac changes during the task supported the efficacy of the threat imminence manipulation in eliciting dissociable defensive states, with faster responses and increased heart rate during imminent compared to distal threats. Individual differences in empathic concern were specifically correlated with helping during imminent threats. These results suggest that defensive states driving active escape from immediate danger may also facilitate decisions to help others, potentially by engaging neurocognitive systems implicated in caregiving across mammals.

Intact Classical Fear Conditioning to Interpersonally Threatening Stimuli in Borderline Personality Disorder.

Threat hypersensitivity is regarded as a central mechanism of deficient emotion regulation, a core feature of patients with borderline personality disorder (BPD). Here, we employed a classical fear-conditioning protocol in which interpersonally threatening, interpersonally non-threatening, and non-social (neutral) visual stimuli were predictive of an aversive auditory stimulus in a sample of 23 medication-free adult female patients with BPD and 21 age- and IQ-matched healthy women. The results did not confirm the hypothesized enhanced and prolonged conditioned skin conductance responses (SCR) and subjective stress and expectancy ratings to interpersonally threatening stimuli in patients with BPD compared to healthy women. Patients with BPD generally expected the aversive stimulus more often irrespective of stimulus category and conditioning. Furthermore, patients with BPD showed larger conditioned SCR to interpersonally non-threatening and neutral than interpersonally threatening stimuli, while interpersonally threatening stimuli elicited higher SCR compared to non-threatening or neutral stimuli in healthy controls. Together with previous studies, the results suggest no alterations in fear conditioning to generally aversive stimuli in BPD. Further studies using stimuli with BPD-specific topics, such as abandonment or rejection, and/or to investigate more interpersonal forms of learning, such as observational or instructed conditioning, are urgently needed to further elucidate the mechanisms involved in the etiology and maintenance of threat hypersensitivity in BPD.

Development of an automated, GMP compliant FASTlab™ radiosynthesis of [18 F]GE-179 for the clinical study of activated NMDA receptors.

N-(2-chloro-5-(S-2-[18 F]fluoroethyl)thiophenyl)-N'-(3-thiomethylphenyl)-N'-methylguanidine, ([18 F]GE-179), has been identified as a promising positron emission tomography (PET) ligand for the intra-channel phencyclidine (PCP) binding site of the N-methyl-D-aspartate (NMDA) receptor. The radiosynthesis of [18 F]GE-179 has only been performed at low radioactivity levels. However, the manufacture of a GMP compliant product at high radioactivity levels was required for clinical studies. We describe the development of a process using the GE FASTlab™ radiosynthesis platform coupled with HPLC purification. The radiosynthesis is a two-step process, involving the nucleophilic fluorination of ethylene ditosylate, 11, followed by alkylation to the deprotonated thiol precursor, N-(2-chloro-5-thiophenol)-N'-(3-thiomethylphenyl)-N'-methyl guanidine, 8. The crude product was purified by semi-preparative HPLC to give the formulated product in an activity yield (AY) of 7 ± 2% (n = 15) with a total synthesis time of 120 minutes. The radioactive concentration (RAC) and radiochemical purity (RCP) were 328 ± 77 MBq/mL and 96.5 ± 1% respectively and the total chemical content was 2 ± 1 µg. The final formulation volume was 14 mL. The previously described radiosynthesis of [18 F]GE-179 was successfully modified to deliver an process on the FASTlab™ that allows the manufacture of a GMP quality product from high starting radioactivitity (up to 80 GBq) and delivers a product suitable for clinical use.

A common neural network differentially mediates direct and social fear learning.

Across species, fears often spread between individuals through social learning. Yet, little is known about the neural and computational mechanisms underlying social learning. Addressing this question, we compared social and direct (Pavlovian) fear learning showing that they showed indistinguishable behavioral effects, and involved the same cross-modal (self/other) aversive learning network, centered on the amygdala, the anterior insula (AI), and the anterior cingulate cortex (ACC). Crucially, the information flow within this network differed between social and direct fear learning. Dynamic causal modeling combined with reinforcement learning modeling revealed that the amygdala and AI provided input to this network during direct and social learning, respectively. Furthermore, the AI gated learning signals based on surprise (associability), which were conveyed to the ACC, in both learning modalities. Our findings provide insights into the mechanisms underlying social fear learning, with implications for understanding common psychological dysfunctions, such as phobias and other anxiety disorders.

Vicarious Fear Learning Depends on Empathic Appraisals and Trait Empathy.

Empathy and vicarious learning of fear are increasingly understood as separate phenomena, but the interaction between the two remains poorly understood. We investigated how social (vicarious) fear learning is affected by empathic appraisals by asking participants to either enhance or decrease their empathic responses to another individual (the demonstrator), who received electric shocks paired with a predictive conditioned stimulus. A third group of participants received no appraisal instructions and responded naturally to the demonstrator. During a later test, participants who had enhanced their empathy evinced the strongest vicarious fear learning as measured by skin conductance responses to the conditioned stimulus in the absence of the demonstrator. Moreover, this effect was augmented in observers high in trait empathy. Our results suggest that a demonstrator's expression can serve as a "social" unconditioned stimulus (US), similar to a personally experienced US in Pavlovian fear conditioning, and that learning from a social US depends on both empathic appraisals and the observers' stable traits.

Neural correlates of biased social fear learning and interaction in an intergroup context.

Associations linking a fearful experience to a member of a social group other than one's own (out-group) are more resistant to change than corresponding associations to a member of one's own (in-group) (Olsson et al., 2005; Kubota et al., 2012), providing a possible link to discriminative behavior. Using a fear conditioning paradigm, we investigated the neural activity underlying aversive learning biases towards in-group (White) and out-group (Black) members, and their predictive value for discriminatory interactive behavior towards novel virtual members of the racial out-group (n=20). Our results indicate that activity in brain regions previously linked to conditioned fear and perception of individuals belonging to the racial out-groups, or otherwise stigmatized groups, jointly contribute to the expression of race-based biases in learning and behavior. In particular, we found that the amygdala and anterior insula (AI) played key roles in differentiating between in-group and out-group faces both when the faces were paired with an aversive event (acquisition) and when no more shocks were administered (extinction). In addition, functional connectivity between the amygdala and the fusiform gyrus increased during perception of conditioned out-group faces. Moreover, we showed that brain activity in the fear-learning-bias network was related to participants' discriminatory interactions with novel out-group members on a later day. Our findings are the first to identify the neural mechanism of fear learning biases towards out-group members, and its relationship to interactive behavior. Our findings provide important clues towards understanding the mechanisms underlying biases between social groups.

Social learning of fear and safety is determined by the demonstrator's racial group.

Social learning offers an efficient route through which humans and other animals learn about potential dangers in the environment. Such learning inherently relies on the transmission of social information and should imply selectivity in what to learn from whom. Here, we conducted two observational learning experiments to assess how humans learn about danger and safety from members ('demonstrators') of an other social group than their own. We show that both fear and safety learning from a racial in-group demonstrator was more potent than learning from a racial out-group demonstrator.

Racial bias shapes social reinforcement learning.

Both emotional facial expressions and markers of racial-group belonging are ubiquitous signals in social interaction, but little is known about how these signals together affect future behavior through learning. To address this issue, we investigated how emotional (threatening or friendly) in-group and out-group faces reinforced behavior in a reinforcement-learning task. We asked whether reinforcement learning would be modulated by intergroup attitudes (i.e., racial bias). The results showed that individual differences in racial bias critically modulated reinforcement learning. As predicted, racial bias was associated with more efficiently learned avoidance of threatening out-group individuals. We used computational modeling analysis to quantitatively delimit the underlying processes affected by social reinforcement. These analyses showed that racial bias modulates the rate at which exposure to threatening out-group individuals is transformed into future avoidance behavior. In concert, these results shed new light on the learning processes underlying social interaction with racial-in-group and out-group individuals.

The convergence between defence and care in mammals.

The motivations to protect oneself and others have often been seen as conflicting. Here, we discuss recent evidence that self-defensive mechanisms may in fact be recruited to enable the helping of others. In some instances, the defensive response to a threat may even be more decisive in promoting helping than the response to a conspecific's distress (as predicted by empathy-altruism models). In light of this evidence, we propose that neural mechanisms implicated in self-defence may have been repurposed through evolution to enable the protection of others, and that defence and care may be convergent rather than conflicting functions. Finally, we present and discuss a working model of the shared brain mechanisms implicated in defence of both self and others.

The transfer of social threat learning to decision making is robust to extinction.

Through traditional mass media and online social media, we are almost constantly exposed to second-hand experiences of trauma and violence, providing ample opportunities for us to learn about threats through social means. This social threat learning can influence instrumental decision making through a social learning to decision-making transfer process, resembling the so-called Pavlovian to instrumental transfer effect, resulting in consequences that can be maladaptive. Here, we assessed if this influence could be diminished by extinction learning, a procedure where a previously threatening stimulus is learned to be safe, and thereby mitigate possible maladaptive consequences. To this end, we recruited 251 participants to undergo a social threat learning procedure (where they observed someone else receive electric shocks to one out of two images), followed by either a social or direct extinction procedure (in which no shocks were given), before conducting an instrumental decision-making task to measure the strength of the transfer effect. Based on theoretical considerations and previous literature, we proposed two competing hypotheses: (a) extinction learning would diminish the transfer effect or (b) the transfer effect would be robust to extinction. Our results clearly demonstrate that the social to instrumental transfer effect is remarkedly robust to extinction, supporting the second hypotheses. Irrespective of whether extinction was carried out through direct experience or social means, learning about threats through second-hand aversive experiences strongly influence instrumental behavior, suggesting that potentially maladaptive effects of social threat learning are challenging to diminish. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Other people as means to a safe end: vicarious extinction blocks the return of learned fear.

Information about what is dangerous and safe in the environment is often transferred from other individuals through social forms of learning, such as observation. Past research has focused on the observational, or vicarious, acquisition of fears, but little is known about how social information can promote safety learning. To address this issue, we studied the effects of vicarious-extinction learning on the recovery of conditioned fear. Compared with a standard extinction procedure, vicarious extinction promoted better extinction and effectively blocked the return of previously learned fear. We confirmed that these effects could not be attributed to the presence of a learning model per se but were specifically driven by the model's experience of safety. Our results confirm that vicarious and direct emotional learning share important characteristics but that social-safety information promotes superior down-regulation of learned fear. These findings have implications for emotional learning, social-affective processes, and clinical practice.