ABSTRACT
Accounts of shared representations posit that the experience of pain and pain empathy rely on similar neural mechanisms. Experimental research employing novel analytical and methodological approaches has made significant advances in both the identification and targeted manipulation of such shared experiences and their neural underpinnings. This revealed that painful experiences can be shared on different representational levels, from pain-specific to domain-general features, such as negative affect and its regulation. In view of direct links between such representations and social behaviors such as prosocial behavior, conditions characterized by aberrant pain processing may come along with heavy impairments in the social domain, depending on the affected representational level. This has wide potential implications in light of the high prevalence of pain-related clinical conditions, their management, and the overuse of pain medication. In this review and opinion paper, we aim to chart the path toward a better understanding of the link between shared affect and prosocial behavior.
Subject(s)
Empathy , Pain , Social Behavior , Humans , Empathy/physiology , Pain/psychology , Pain/physiopathology , Pain Perception/physiology , Brain/physiopathology , Brain/physiology , Clinical RelevanceABSTRACT
Many everyday decisions, including those concerning our health, finances and the environment, involve choosing between a smaller but imminent reward (e.g., 20 now) and a later but larger reward (e.g., 40 in a month). The extent to which an individual prefers smaller imminent rewards over larger delayed rewards can be measured using delay discounting tasks. Acute stress induces a cascade of biological and psychological responses with potential consequences for how individuals think about the future, process rewards, and make decisions, all of which can impact delay discounting. Several studies have shown that individuals focus more on imminent rewards under stress. These findings have been used to explain why individuals make detrimental choices under acute stress. Yet, the evidence linking acute stress to delay discounting is equivocal. To address this uncertainty, we conducted a meta-analysis of 11 studies (14 effects) to systematically quantify the effects of acute stress on monetary delay discounting. Overall, we find no effect of acute stress on delay discounting, compared to control conditions (SMD = -0.18, 95% CI [-0.57, 0.20], p = 0.32). We also find that neither the gender/sex of the participants, the type of stressor (e.g., physical vs. psychosocial) nor whether monetary decisions were hypothetical or incentivized (i.e. monetary decisions were actually paid out) moderated the impact of acute stress on monetary delay discounting. We argue that establishing the effects of acute stress on the separate processes involved in delay discounting, such as reward valuation and prospection, will help to resolve the inconsistencies in the field.
ABSTRACT
Dogs and humans have lived together for thousands of years and share many analogous socio-cognitive skills. Dog neuroimaging now provides insight into the neural bases of these shared social abilities. Here, we summarize key findings from dog fMRI identifying neocortical brain areas implicated in visual social cognition, such as face, body, and emotion perception, as well as action observation in dogs. These findings provide converging evidence that the temporal cortex plays a significant role in visual social cognition in dogs. We further briefly review investigations into the neural base of the dog-human relationship, mainly involving limbic brain regions. We then discuss current challenges in the field, such as statistical power and lack of common template spaces, and how to overcome them. Finally, we argue that the foundation has now been built to investigate and compare the neural bases of more complex socio-cognitive phenomena shared by dogs and humans. This will strengthen and expand the role of the domestic dog as a powerful comparative model species and provide novel insights into the evolutionary roots of social cognition.
Subject(s)
Social Cognition , Animals , Dogs , Humans , Neurosciences , Brain/physiology , Models, Animal , Magnetic Resonance Imaging , Social BehaviorABSTRACT
Dogs are increasingly used as a model for neuroscience due to their ability to undergo functional MRI fully awake and unrestrained, after extensive behavioral training. Still, we know rather little about dogs' basic functional neuroanatomy, including how basic perceptual and motor functions are localized in their brains. This is a major shortcoming in interpreting activations obtained in dog fMRI. The aim of this preregistered study was to localize areas associated with somatosensory processing. To this end, we touched N = 22 dogs undergoing fMRI scanning on their left and right flanks using a wooden rod. We identified activation in anatomically defined primary and secondary somatosensory areas (SI and SII), lateralized to the contralateral hemisphere depending on the side of touch, and importantly also activation beyond SI and SII, in the cingulate cortex, right cerebellum and vermis, and the sylvian gyri. These activations may partly relate to motor control (cerebellum, cingulate), but also potentially to higher-order cognitive processing of somatosensory stimuli (rostral sylvian gyri), and the affective aspects of the stimulation (cingulate). We also found evidence for individual side biases in a vast majority of dogs in our sample, pointing at functional lateralization of somatosensory processing. These findings not only provide further evidence that fMRI is suited to localize neuro-cognitive processing in dogs, but also expand our understanding of in vivo touch processing in mammals, beyond classically defined primary and secondary somatosensory cortices.
Subject(s)
Brain Mapping , Magnetic Resonance Imaging , Somatosensory Cortex , Animals , Dogs , Magnetic Resonance Imaging/methods , Somatosensory Cortex/physiology , Somatosensory Cortex/diagnostic imaging , Brain Mapping/methods , Male , Female , Wakefulness/physiology , Functional Laterality/physiology , Touch/physiology , Touch Perception/physiology , Physical StimulationABSTRACT
The ability to make sense of and predict others' actions is foundational for many socio-cognitive abilities. Dogs (Canis familiaris) constitute interesting comparative models for the study of action perception due to their marked sensitivity to human actions. We tested companion dogs (N = 21) in two screen-based eye-tracking experiments, adopting a task previously used with human infants and apes, to assess which aspects of an agent's action dogs consider relevant to the agent's underlying intentions. An agent was shown repeatedly acting upon the same one of two objects, positioned in the same location. We then presented the objects in swapped locations and the agent approached the objects centrally (Experiment 1) or the old object in the new location or the new object in the old location (Experiment 2). Dogs' anticipatory fixations and looking times did not reflect an expectation that agents should have continued approaching the same object nor the same location as witnessed during the brief familiarization phase; this contrasts with some findings with infants and apes, but aligns with findings in younger infants before they have sufficient motor experience with the observed action. However, dogs' pupil dilation and latency to make an anticipatory fixation suggested that, if anything, dogs expected the agents to keep approaching the same location rather than the same object, and their looking times showed sensitivity to the animacy of the agents. We conclude that dogs, lacking motor experience with the observed actions of grasping or kicking performed by a human or inanimate agent, might interpret such actions as directed toward a specific location rather than a specific object. Future research will need to further probe the suitability of anticipatory looking as measure of dogs' socio-cognitive abilities given differences between the visual systems of dogs and primates.
Subject(s)
Cognition , Hominidae , Humans , Dogs , AnimalsABSTRACT
Acute stress can change our cognition and emotions, but what specific consequences this has for human prosocial behaviour is unclear. Previous studies have mainly investigated prosociality with financial transfers in economic games and produced conflicting results. Yet a core feature of many types of prosocial behaviour is that they are effortful. We therefore examined how acute stress changes our willingness to exert effort that benefits others. Healthy male participants - half of whom were put under acute stress - made decisions whether to exert physical effort to gain money for themselves or another person. With this design, we could independently assess the effects of acute stress on prosocial, compared to self-benefitting, effortful behaviour. Compared to controls (n = 45), participants in the stress group (n = 46) chose to exert effort more often for self- than for other-benefitting rewards at a low level of effort. Additionally, the adverse effects of stress on prosocial effort were particularly pronounced in more selfish participants. Neuroimaging combined with computational modelling revealed a putative neural mechanism underlying these effects: more stressed participants showed increased activation to subjective value in the dorsal anterior cingulate cortex and anterior insula when they themselves could benefit from their exerted effort relative to when someone else could. By using an effort-based task that better approximates real-life prosocial behaviour and incorporating trait differences in prosocial tendencies, our study provides important insights into how acute stress affects prosociality and its associated neural mechanisms.
Subject(s)
Altruism , Drug-Related Side Effects and Adverse Reactions , Humans , Male , Cognition , Computer Simulation , EmotionsABSTRACT
BACKGROUND: Social touch is an integral part of social relationships and has been associated with reward. Major depressive disorder (MDD) is characterized by severe impairments in reward processing, but the neural effects of social touch in MDD are still elusive. In this study, we aimed to determine whether the neural processing of social touch is altered in MDD and to assess the impact of antidepressant therapy. METHODS: Before and after antidepressant treatment, 53 MDD patients and 41 healthy controls underwent functional magnetic resonance imaging (fMRI) while receiving social touch. We compared neural responses to social touch in the reward network, behavioral ratings of touch comfort and general aversion to interpersonal touch in patients to controls. Additionally, we examined the effect of treatment response on those measures. RESULTS: Clinical symptoms decreased after treatment and 43.4% of patients were classified as responders. Patients reported higher aversion to interpersonal touch and lower comfort ratings during the fMRI paradigm than controls. Patients showed reduced responses to social touch in the nucleus accumbens, caudate nucleus and putamen than controls, both before and after treatment. Contrary to our hypotheses, these effects were independent of touch velocity. Non-responders exhibited blunted response in the caudate nucleus and the insula compared to responders, again irrespective of time. CONCLUSIONS: These findings suggest altered striatal processing of social touch in MDD. Persistent dysfunctional processing of social touch despite clinical improvements may constitute a latent risk factor for social withdrawal and isolation.
Subject(s)
Depressive Disorder, Major , Humans , Depressive Disorder, Major/drug therapy , Touch , Depression , Reward , Antidepressive Agents/therapeutic use , Magnetic Resonance ImagingABSTRACT
Finding ways to investigate false belief understanding nonverbally is not just important for preverbal children but also is the only way to assess theory of mind (ToM)-like abilities in nonhuman animals. In this preregistered study, we adapted the design from a previous study on pet dogs to investigate false belief understanding in children and to compare it with belief understanding of those previously tested dogs. A total of 32 preschool children (aged 5-6 years) saw the displacement of a reward and obtained nonverbal cueing of the empty container from an adult communicator holding either a true or false belief. In the false belief condition, when the communicator did not know the location of the reward, children picked the baited container, but not the cued container, more often than the empty one. In the true belief condition, when the communicator witnessed the displacement yet still cued the wrong container, children performed randomly. The children's behavior pattern was at odds with that of the dogs tested in a previous study, which picked the cued container more often when the human communicator held a false belief. In addition to species comparisons, because our task does not require verbal responses or relational sentence understanding, it can also be used in preverbal children. The children in our study behaved in line with the existing ToM literature, whereas most (but not all) dogs from the previously collected sample, although sensitive to differences between the belief conditions, deviated from the children. This difference suggests that using closely matched paradigms and experimental procedures can reveal decisive differences in belief processing between species. It also demonstrates the need for a more comprehensive exploration and direct comparison of the various aspects of false belief processing and ToM in different species to understand the evolution of social cognition.
Subject(s)
Comprehension , Theory of Mind , Adult , Child, Preschool , Humans , Animals , Dogs , Comprehension/physiology , Cues , CommunicationABSTRACT
The amygdala is a heterogeneous network of subcortical nuclei with central importance in cognitive and clinical neuroscience. Various experimental designs in human psychology and animal model research have mapped multiple conceptual frameworks (e.g., valence/salience and decision making) to ever more refined amygdala circuitry. However, these predominantly bottom up-driven accounts often rely on interpretations tailored to a specific phenomenon, thus preventing comprehensive and integrative theories. We argue here that an active inference model of amygdala function could unify these fractionated approaches into an overarching framework for clearer empirical predictions and mechanistic interpretations. This framework embeds top-down predictive models, informed by prior knowledge and belief updating, within a dynamical system distributed across amygdala circuits in which self-regulation is implemented by continuously tracking environmental and homeostatic demands.
Subject(s)
Amygdala , Emotions , Humans , Animals , Amygdala/physiology , Emotions/physiologyABSTRACT
Influential accounts claim that violent video games (VVGs) decrease players' emotional empathy by desensitizing them to both virtual and real-life violence. However, scientific evidence for this claim is inconclusive and controversially debated. To assess the causal effect of VVGs on the behavioral and neural correlates of empathy and emotional reactivity to violence, we conducted a prospective experimental study using functional magnetic resonance imaging (fMRI). We recruited 89 male participants without prior VVG experience. Over the course of two weeks, participants played either a highly violent video game or a non-violent version of the same game. Before and after this period, participants completed an fMRI experiment with paradigms measuring their empathy for pain and emotional reactivity to violent images. Applying a Bayesian analysis approach throughout enabled us to find substantial evidence for the absence of an effect of VVGs on the behavioral and neural correlates of empathy. Moreover, participants in the VVG group were not desensitized to images of real-world violence. These results imply that short and controlled exposure to VVGs does not numb empathy nor the responses to real-world violence. We discuss the implications of our findings regarding the potential and limitations of experimental research on the causal effects of VVGs. While VVGs might not have a discernible effect on the investigated subpopulation within our carefully controlled experimental setting, our results cannot preclude that effects could be found in settings with higher ecological validity, in vulnerable subpopulations, or after more extensive VVG play.
Violent video games have often been accused of facilitating aggressive behaviour, in particular due to concerns that they could numb players toward real violence and therefore result in decreased empathy towards the pain of others. However, studies investigating these claims have often produced conflicting results, potentially due to methodological issues. For instance, work showing that violent games lead to emotional desensitization has often relied on testing participants immediately after a gaming session, which limits interpretations about prolonged impact. Many studies also compare gamers to people with no gaming experience, making it difficult to assess whether violent games decrease empathy, or whether less empathetic individuals are more likely to be drawn to this content. Lengersdorff et al. aimed to examine the long-term effects of violent video games using an experimental design that would bypass some of these limitations. A group of 89 young men with little gaming experience were recruited to play either a highly or non-violent version of the same game for seven hour-long sessions over two weeks. The way their brain reacted to violent images and processed other people's pain was assessed before and after this 'gaming training' using fMRI. The analyses showed no changes in these measures in volunteers who played the violent version of the game, suggesting that it had not numbed them to violence or affected their empathy. While experimental studies cannot fully capture the experiences of real-world gamers, the findings by Lengersdorff et al. represent a step towards resolving the scientific controversy surrounding the effects of violent games. Ultimately, a deeper understanding of how this type of media influences our emotions could help inform policymaking decisions about access to violent content.
Subject(s)
Empathy , Video Games , Humans , Male , Bayes Theorem , Prospective Studies , Violence/psychology , Aggression/psychology , Video Games/psychology , Neuroimaging , PainABSTRACT
The ability to predict others' actions is one of the main pillars of social cognition. We investigated the processes underlying this ability by pitting motor representations of the observed movements against visual familiarity. In two pre-registered eye-tracking experiments, we measured the gaze arrival times of 16 dogs (Canis familiaris) who observed videos of a human or a conspecific executing the same goal-directed actions. On the first trial, when the human agent performed human-typical movements outside dogs' specific motor repertoire, dogs' gaze arrived at the target object anticipatorily (i.e., before the human touched the target object). When the agent was a conspecific, dogs' gaze arrived to the target object reactively (i.e., upon or after touch). When the human agent performed unusual movements more closely related to the dogs' motor possibilities (e.g., crawling instead of walking), dogs' gaze arrival times were intermediate between the other two conditions. In a replication experiment, with slightly different stimuli, dogs' looks to the target object were neither significantly predictive nor reactive, irrespective of the agent. However, when including looks at the target object that were not preceded by looks to the agents, on average dogs looked anticipatorily and sooner at the human agent's action target than at the conspecific's. Looking times and pupil size analyses suggest that the dogs' attention was captured more by the dog agent. These results suggest that visual familiarity with the observed action and saliency of the agent had a stronger influence on the dogs' looking behaviour than effector-specific movement representations in anticipating action targets.
ABSTRACT
Introduction: Placebo responsiveness is highly variable across individuals. In the domain of pain, it may range from pronounced hypoalgesia to no response at all. Which factors predict such variation awaits clarification, as the available literature is characterized by mixed and inconclusive results. Particularly interesting in this case are social factors such as empathy or prosocial behavior, as prior work has stressed the connection between feeling pain yourself and empathizing with pain observed in others. Methods: In a mixed confirmatory and exploratory approach, this study investigated potential psychological and structural brain differences between placebo responders and non-responders in the domain of pain. We aggregated data of four behavioral and neuroimaging studies that had been designed to investigate the effects of placebo analgesia on empathy. Results: Analyses comparing groups of placebo responders and non-responders showed significant group differences in trait characteristics, with responders reporting increased helping behavior and lower psychopathic traits compared to non-responders. Uncorrected results further showed higher pain-related empathic concern in responders vs. non-responders. These results were accompaniedby tentative group differences in brain structure: placebo analgesia non-responders exhibited increased gray matter volume in left inferior temporal and parietal supramarginal cortical areas, and an increased cortical surface area in bilateral middle temporal cortex. Discussion: Together, our findings suggest that modifiability of one's pain perception by means of placebo effects is linked to personality traits characterizing social emotions and behavior. They also hint that these psychological as well as brain structural characteristics might be beneficial for the identification of placebo responders. At the same time, they stress the importance of considering contextual factors such as the study setting or paradigm when investigating the association between individual characteristics and placebo responding.
ABSTRACT
Previous research has demonstrated a link between the administration of analgesic drugs and the reduction of empathy levels in humans. This apparent blunting effect of pain medication has been explained through shared neural mechanisms for the first-hand and the empathic experience of pain (simulation theory). Considering that analgesics are among the most consumed drugs in the world and the ability to empathize with others is fundamental to human social interactions, the aim of the present study was to investigate whether the typical day-to-day analgesic consumption rate in Austria and Germany is associated with a reduction in empathy and prosocial behavior. We therefore collected self-reports of analgesic consumption behavior as well as empathy for pain and prosocial behavior measures in an online survey (n = 940). Analyses revealed no significant association between the analgesic intake frequency and measures of empathy or prosocial behavior. However, liberal intake of analgesics (i.e. mind-set of "a pill is a quick solution") was linked to lower empathic concern and helping behavior, which may hint towards a negative effect in people who take pain medication for non-pain related issues or episodes of low pain. Nevertheless, further research is needed to investigate the effects of analgesic drugs in high frequency users.
Subject(s)
Altruism , Empathy , Humans , Social Behavior , Pain/drug therapy , Helping Behavior , AnalgesicsABSTRACT
The ability to learn about other people is crucial for human social functioning. Dopamine has been proposed to regulate the precision of beliefs, but direct behavioural evidence of this is lacking. In this study, we investigate how a high dose of the D2/D3 dopamine receptor antagonist sulpiride impacts learning about other people's prosocial attitudes in a repeated Trust game. Using a Bayesian model of belief updating, we show that in a sample of 76 male participants sulpiride increases the volatility of beliefs, which leads to higher precision weights on prediction errors. This effect is driven by participants with genetically conferred higher dopamine availability (Taq1a polymorphism) and remains even after controlling for working memory performance. Higher precision weights are reflected in higher reciprocal behaviour in the repeated Trust game but not in single-round Trust games. Our data provide evidence that the D2 receptors are pivotal in regulating prediction error-driven belief updating in a social context.
Subject(s)
Dopamine Antagonists , Sulpiride , Humans , Male , Dopamine , Trust , Bayes Theorem , Receptors, Dopamine D3/genetics , Receptors, Dopamine D2ABSTRACT
Comparing the neural correlates of socio-cognitive skills across species provides insights into the evolution of the social brain and has revealed face- and body-sensitive regions in the primate temporal lobe. Although from a different lineage, dogs share convergent visuo-cognitive skills with humans and a temporal lobe which evolved independently in carnivorans. We investigated the neural correlates of face and body perception in dogs (N = 15) and humans (N = 40) using functional MRI. Combining univariate and multivariate analysis approaches, we found functionally analogous occipito-temporal regions involved in the perception of animate entities and bodies in both species and face-sensitive regions in humans. Though unpredicted, we also observed neural representations of faces compared to inanimate objects, and dog compared to human bodies in dog olfactory regions. These findings shed light on the evolutionary foundations of human and dog social cognition and the predominant role of the temporal lobe.
Subject(s)
Brain Mapping , Pattern Recognition, Visual , Humans , Dogs , Animals , Temporal Lobe/diagnostic imaging , Brain , FaceABSTRACT
Humans tend to automatically imitate others and their actions while also being able to control such imitative tendencies. Interference control, necessary to suppress own imitative tendencies, develops rapidly in childhood and adolescence, plateaus in adulthood and slowly declines with advancing age. It remains to be shown though which neural processes underpin these differences across the lifespan. In a cross-sectional functional magnetic resonance imaging study with three age groups (adolescents (ADs) 14-17 years, young adults (YAs) 21-31, older adults (OAs) 56-76, N = 91 healthy female participants), we investigated the behavioral and neural correlates of interference control in the context of automatic imitation using the finger-lifting task. ADs showed the most efficient interference control, while no significant differences emerged between YAs and OAs, despite OAs showing longer reaction times. On the neural level, all age groups showed engagement of the right temporoparietal junction, right supramarginal gyrus and bilateral insula, aligning well with studies previously using this task. However, our analyses did not reveal any age-related differences in brain activation, neither in these nor in other areas. This suggests that ADs might have a more efficient use of the engaged brain networks and, on the other hand, OAs' capacity for interference control and the associated brain functions might be largely preserved.
Subject(s)
Lifting , Magnetic Resonance Imaging , Young Adult , Adolescent , Humans , Female , Aged , Cross-Sectional Studies , Brain/diagnostic imaging , Brain/physiology , Reaction Time , Brain MappingABSTRACT
The COVID-19 pandemic has affected all domains of human life, including the economic and social fabric of societies. One of the central strategies for managing public health throughout the pandemic has been through persuasive messaging and collective behaviour change. To help scholars better understand the social and moral psychology behind public health behaviour, we present a dataset comprising of 51,404 individuals from 69 countries. This dataset was collected for the International Collaboration on Social & Moral Psychology of COVID-19 project (ICSMP COVID-19). This social science survey invited participants around the world to complete a series of moral and psychological measures and public health attitudes about COVID-19 during an early phase of the COVID-19 pandemic (between April and June 2020). The survey included seven broad categories of questions: COVID-19 beliefs and compliance behaviours; identity and social attitudes; ideology; health and well-being; moral beliefs and motivation; personality traits; and demographic variables. We report both raw and cleaned data, along with all survey materials, data visualisations, and psychometric evaluations of key variables.
Subject(s)
COVID-19 , Humans , Attitude , COVID-19/psychology , Morals , Pandemics , Surveys and Questionnaires , Social Change , Socioeconomic FactorsABSTRACT
Humans are strategically more prosocial when their actions are being watched by others than when they act alone. Using a psychopharmacogenetic approach, we investigated the endocrinological and computational mechanisms of such audience-driven prosociality. One hundred and ninety-two male participants received either a single dose of testosterone (150 mg) or a placebo and performed a prosocial and self-benefitting reinforcement learning task. Crucially, the task was performed either in private or when being watched. Rival theories suggest that the hormone might either diminish or strengthen audience-dependent prosociality. We show that exogenous testosterone fully eliminated strategic, i.e., feigned, prosociality and thus decreased submission to audience expectations. We next performed reinforcement-learning drift-diffusion computational modeling to elucidate which latent aspects of decision-making testosterone acted on. The modeling revealed that testosterone compared to placebo did not deteriorate reinforcement learning per se. Rather, when being watched, the hormone altered the degree to which the learned information on choice value translated to action selection. Taken together, our study provides novel evidence of testosterone's effects on implicit reward processing, through which it counteracts conformity and deceptive reputation strategies.
Subject(s)
Altruism , Testosterone , Humans , Male , Choice Behavior , Reinforcement, Psychology , Reward , Social Behavior , Testosterone/pharmacologyABSTRACT
Seminal studies suggest that being mimicked increases experienced social closeness and prosocial behavior to a mimicking confederate (i.e., interaction partner). Here we reexamine these results by considering the role of empathy-related traits, an indirect proxy for endorphin uptake, and their combined effects as an explanation for these results. 180 female participants were mimicked or anti-mimicked in an interaction with a confederate. The effects of being mimicked versus anti-mimicked in relation to empathy-related traits and endorphin release (assessed indirectly via pain tolerance) on experienced closeness and prosocial behavior were assessed using Bayesian analyses. Our results suggest that high individual empathy-related traits increase social closeness to the anti-mimicking and mimicking confederate and to one's romantic partner, as compared to mimicry alone. Results furthermore strongly suggest that high individual empathy-related traits increase prosocial behavior (donations and willingness to help) as compared to mimicry alone. These findings extend previous work by highlighting that empathy-related traits are more influential in creating positive effects on social closeness and prosocial behavior than a one-shot mimicking encounter.