Benjamin A. Tabak

Cognitive systems for revenge and forgiveness

Minimizing the costs that others impose upon oneself and upon those in whom one has a fitness stake, such as kin and allies, is a key adaptive problem for many organisms. Our ancestors regularly faced such adaptive problems (including homicide, bodily harm, theft, mate poaching, cuckoldry, reputational damage, sexual aggression, and the infliction of these costs on one’s offspring, mates, coalition partners, or friends). One solution to this problem is to impose retaliatory costs on an aggressor so that the aggressor and other observers will lower their estimates of the net benefits to be gained from exploiting the retaliator in the future. We posit that humans have an evolved cognitive system that implements this strategy – deterrence – which we conceptualize as a revenge system. The revenge system produces a second adaptive problem: losing downstream gains from the individual on whom retaliatory costs have been imposed. We posit, consequently, a subsidiary computational system designed to restore particular relationships after cost-imposing interactions by inhibiting revenge and motivating behaviors that signal benevolence for the harmdoer. The operation of these systems depends on estimating the risk of future exploitation by the harmdoer and the expected future value of the relationship with the harmdoer. We review empirical evidence regarding the operation of these systems, discuss the causes of cultural and individual differences in their outputs, and sketch their computational architecture.

Evaluation of enzyme immunoassay and radioimmunoassay methods for the measurement of plasma oxytocin

Objective: There is increased interest in measuring peripheral oxytocin levels to better understand the role of this peptide in mammalian behavior, physiology, and disease. The purpose of this study was to compare methods for plasma oxytocin measurement using a commercially available enzyme immunoassay (EIA) and radioimmunoassay (RIA), to evaluate the need for sample extraction, and to assess the immunospecificity of the assays. Methods: Oxytocin was measured in extracted and unextracted human plasma samples (n = 39). Oxytocin and its degradation products were separated by high-performance liquid chromatography and gel filtration chromatography and then assayed by EIA or RIA to identify oxytocin immunoreactive peaks. Results: Without extraction, plasma measured by EIA was more than 100-fold higher than in extracted plasma, and the correlation between oxytocin levels in extracted and unextracted plasma was minimal (Spearman &rgr; = −0.10, p = .54). Using the RIA, most samples (>90%) were below the level of detection with or without extraction. After chromatographic fractionation of sample extracts, multiple immunoreactive products were found to be present in addition to oxytocin, which casts doubts on the specificity of the assays. Conclusions: Changes in oxytocin levels have been reported in social and behavioral challenge studies. This study indicates that sample extraction is necessary to obtain valid assay results. Changes in oxytocin degradation products are likely to contribute to the previously observed responses in circulating oxytocin levels to behavioral and social challenge. There is a critical need for valid and reliable methods to measure oxytocin in biologic samples.Abbreviations: EIA = enzyme immunoassay; RIA = radioimmunoassay; HPLC = high-performance liquid chromatography; SEM = standard error of the mean; MW = molecular weight

Oxytocin indexes relational distress following interpersonal harms in women

The hypothalamic neuropeptide oxytocin, known for its involvement in social affiliation and bonding in animals, has recently been associated with a host of prosocial behaviors that are beneficial for maintaining positive social relationships in humans. Paradoxically, however, people with high endogenous levels of oxytocin also tend to report relational distress and interpersonal difficulties in their everyday lives. To address these contradictory findings, oxytocin reactivity was measured in response to a well-defined laboratory task in young adult women following recent interpersonal harms. Elevated mean peripheral oxytocin reactivity (but not baseline levels of oxytocin or cortisol reactivity) was associated with increased post-conflict anxiety and decreased levels of forgiveness. These results corroborate previous research implicating oxytocin as a neuroendocrine marker of relational distress, but not general stress, and demonstrate the utility of studying oxytocin in response to naturally occurring relational events.

Vasopressin, but not oxytocin, increases empathic concern among individuals who received higher levels of paternal warmth: A randomized controlled trial

BACKGROUND Empathy improves our ability to communicate in social interactions and motivates prosocial behavior. The neuropeptides arginine vasopressin and oxytocin play key roles in socioemotional processes such as pair bonding and parental care, which suggests that they may be involved in empathic processing. METHODS We investigated how vasopressin and oxytocin affect empathic responding in a randomized, double-blind, placebo controlled, between-subjects study design. We also examined the moderating role of parental warmth, as reported in the early family environment, on empathic responding following vasopressin, oxytocin, or placebo administration. RESULTS Among participants who reported higher levels of paternal warmth (but not maternal warmth), vasopressin (vs. placebo and oxytocin) increased ratings of empathic concern after viewing distressing and uplifting videos. No main or interaction effects were found for individuals who received oxytocin. CONCLUSIONS Vasopressin has a role in enhancing empathy among individuals who received higher levels of paternal warmth. TRIAL REGISTRATION NCT01680718.

Variation in oxytocin receptor gene (OXTR) polymorphisms is associated with emotional and behavioral reactions to betrayal

Variations in the gene that encodes the oxytocin receptor (OXTR) have been associated with many aspects of social cognition as well as several prosocial behaviors. However, potential associations of OXTR variants with reactions to betrayals of trust while cooperating for mutual benefit have not yet been explored. We examined how variations in 10 single-nucleotide polymorphisms on OXTR were associated with behavior and emotional reactions after a betrayal of trust in an iterated Prisoners Dilemma Game. After correction for multiple testing, one haplotype (C-rs9840864, T-rs2268494) was significantly associated with faster retaliation post-betrayal-an association that appeared to be due to this haplotypes intermediate effect of exacerbating peoples anger after they had been betrayed. Furthermore, a second haplotype (A-rs237887, C-rs2268490) was associated with higher levels of post-betrayal satisfaction, and a third haplotype (G-rs237887, C-rs2268490) was associated with lower levels of post-betrayal satisfaction.

Conciliatory gestures promote forgiveness and reduce anger in humans.

Significance Conflict is a common feature of social life among group-living animals, but many social relationships often retain value even after conflicts have occurred. Consequently, natural selection has likely endowed humans and other animal species with cognitive systems that motivate reconciliation with interaction partners that they perceive as valuable and nonthreatening, notwithstanding prior conflict. In a large sample of people who had recently been harmed by an interaction partner, we found that conciliatory gestures, such as apologies and offers of compensation, accelerated forgiveness and reduced anger toward transgressors, largely by altering victims’ perceptions of their transgressors’ relationship value and exploitation risk. These results give insight into the design logic behind the cognitive systems that motivate human postconflict reconciliation. Conflict is an inevitable component of social life, and natural selection has exerted strong effects on many organisms to facilitate victory in conflict and to deter conspecifics from imposing harms upon them. Like many species, humans likely possess cognitive systems whose function is to motivate revenge as a means of deterring individuals who have harmed them from harming them again in the future. However, many social relationships often retain value even after conflicts have occurred between interactants, so natural selection has very likely also endowed humans with cognitive systems whose function is to motivate reconciliation with transgressors whom they perceive as valuable and nonthreatening, notwithstanding their harmful prior actions. In a longitudinal study with 337 participants who had recently been harmed by a relationship partner, we found that conciliatory gestures (e.g., apologies, offers of compensation) were associated with increases in victims’ perceptions of their transgressors’ relationship value and reductions in perceptions of their transgressors’ exploitation risk. In addition, conciliatory gestures appeared to accelerate forgiveness and reduce reactive anger via their intermediate effects on relationship value and exploitation risk. These results strongly suggest that conciliatory gestures facilitate forgiveness and reduce anger by modifying victims’ perceptions of their transgressors’ value as relationship partners and likelihood of recidivism.

Oxytocin and social salience: a call for gene-environment interaction research

The role of the neuropeptide oxytocin in social cognition and prosocial behavior continues to fascinate the scientific community (Bartz et al., 2011b). However, as our knowledge of oxytocins influence on social processes increases, a more complex picture continues to emerge. Studies have begun to identify individual differences and environmental contexts that substantially alter the effects of oxytocin administration (Bartz et al., 2011b; Macdonald, 2012). In addition, interpersonal distress has been positively correlated with plasma oxytocin (e.g., Tabak et al., 2011), and evidence for potential negative consequences of oxytocin administration continues to accumulate (Miller, 2013)—calling into question the view that oxytocin represents a social panacea (Pfeiffer, 2013). Although questions remain about how to properly measure oxytocin (Szeto et al., 2011; McCullough et al., 2013), and whether intranasal administration of oxytocin crosses the blood-brain barrier (Churchland and Winkielman, 2012; but see, Neumann et al., 2013), a developing theme in human oxytocin research is that early environmental experiences and/or attachment styles appear to moderate the effects of oxytocin administration (Bartz et al., 2010, 2011a; van IJzendoorn et al., 2011; De Dreu, 2012a; Riem et al., 2013). Translational research has demonstrated that early environmental experiences can alter the oxytocin system (Champagne et al., 2001; Bales and Perkeybile, 2012), which may have long-lasting effects that impact adult human functioning (e.g., Heim et al., 2009; Strathearn et al., 2009; Feldman et al., 2013). Based on findings such as these, an increasing number of studies have begun to investigate how variation on the gene encoding for the oxytocin receptor (OXTR) may relate to socially relevant normative and pathological phenotypes. To date, the most commonly studied marker on OXTR is rs53576, an adenine-to-guanine single nucleotide polymorphism (SNP) that lies in the third intronic region. Although most published studies have found associations with the rs53576 G allele and beneficial aspects of social cognition and behavior (e.g., Saphire-Bernstein et al., 2011; Krueger et al., 2012), several studies have found no relationship between rs53576 genotype and similar social phenotypes (e.g., Apicella et al., 2010; Cornelis et al., 2012; Tabak et al., 2013), or opposite relationships (i.e., where the A allele is protective; Costa et al., 2009). Although some of these discrepancies likely result from known issues in genetic association studies (e.g., Ioannidis et al., 2001; Lin et al., 2007), findings from studies of endogenous oxytocin (Strathearn et al., 2009), oxytocin administration (van IJzendoorn et al., 2011), and OXTR (McQuaid et al., 2013) suggest that one method through which studies might yield more consistent findings is to include measures of environmental experiences in order to examine gene-environment interactions. In a study recently published in this journal, McQuaid et al. (2013) examined how rs53576 genotype moderated the relationship between childhood maltreatment and depression symptoms in a racially/ethnically diverse sample. The authors found an association between individuals who carried the G allele on rs53576 and increased depression symptomology compared to those with the AA genotype. Furthermore, the authors discovered a meditational role of distrust/cynicism, suggesting that depression symptoms resulted (or co-occurred) in part from developing a distrustful attitude toward others after having suffered childhood maltreatment. McQuaid et al.s 2013 findings are in agreement with Bradley et al. (2011) who studied a larger sample (n = 595) of 18–90 year old African Americans with low-incomes: they found that individuals with the GG genotype on rs53576 who experienced severe childhood maltreatment were more likely to have disorganized attachment styles and higher levels of emotional dysregulation. Thus, in contrast to the majority of published studies focusing on rs53576, Bradley et al. (2011) and McQuaid et al. (2013) found that it was the G allele that represented risk rather than protection when examined in the context of childhood maltreatment. Initially, these findings seem to contradict those from previous studies; however, these results are in agreement with the “social salience” hypothesis of oxytocin, which proposes that oxytocin increases the salience of both positive and negative social cues (Shamay-Tsoory et al., 2009). Following this logic, enhanced social salience may improve social cognition and increase prosocial behavior for individuals in positive environments, but have detrimental effects for others in negative environments (Bartz et al., 2011b; Bakermans-Kranenburg and van IJzendoorn, 2013), perhaps because these environments encourage the view that others are untrustworthy (Bakermans-Kranenburg et al., 2012). This hypothesis has gained some traction in light of recent findings demonstrating that oxytocin does not promote (or reduces) prosocial tendencies toward anonymous others or out-group members (Declerck et al., 2010; De Dreu et al., 2010; Radke and de Bruijn, 2012). However, the ways in which oxytocin administration may differentially affect people depending on attachment anxiety and/or avoidance continue to be explored (Bartz, 2012; De Dreu, 2012b). Findings from Bradley et al. (2011) and McQuaid et al. (2013) involving rs53576 are also in agreement with the differential susceptibility hypothesis (Belsky et al., 2009), which posits that certain genetic variants can represent risk or protection depending upon whether or not the environment is positive or negative (for a discussion of differential susceptibility as related to another OXTR SNP, rs2254298, see Brune, 2012). Importantly, the function of rs53576 is unknown. In addition, results from McQuaid et al. (2013) were based on a cross-sectional design, retrospective self-reports, and a small heterogeneous sample, which increases the potential for false-positive findings (Moffitt et al., 2006). As a result, the authors appropriately note that replication with larger samples and more sophisticated methodology is needed. Nonetheless, results from McQuaid et al. (2013) are in agreement with studies demonstrating the plasticity of the oxytocin system in both animals and humans and suggest that it is in the best interest of researchers investigating genetic associations (as well as epigenetic mechanisms; Kumsta et al., 2013) in oxytocin system relevant genes to measure both positive and negative environmental experiences for the purpose of examining gene-environment interactions.

Putting revenge and forgiveness in an evolutionary context.

In this response, we address eight issues concerning our proposal that human minds contain adaptations for revenge and forgiveness. Specifically, we discuss (a) the inferences that are and are not licensed by patterns of contemporary behavioral data in the context of the adaptationist approach; (b) the theoretical pitfalls of conflating proximate and ultimate causation; (c) the role of development in the production of adaptations; (d) the implications of proposing that the brain’s cognitive systems are fundamentally computational in nature; (e) our preferred method for considering the role of individual differences in computational systems; (f) applications of our proposal to understanding conflicts between groups; (g) the possible implications of our views for understanding the operation of contemporary criminal justice systems; and (h) the question of whether people ever “genuinely” forgive.

Oxytocin, but not vasopressin, impairs social cognitive ability among individuals with higher levels of social anxiety: A randomized controlled trial

Individuals with social anxiety are characterized by a high degree of social sensitivity, which can coincide with impairments in social cognitive functioning (e.g. theory of mind). Oxytocin (OT) and vasopressin (AVP) have been shown to improve social cognition, and OT has been theorized as a potential therapeutic agent for individuals with social anxiety disorder. However, no study has investigated whether these neuropeptides improve social cognitive ability among socially anxious individuals. In a randomized, double-blind, placebo controlled, between-subjects design we investigated whether social anxiety moderated the effects of OT or AVP (vs placebo) on social working memory (i.e. working memory that involves manipulating social information) and non-social working memory. OT vs placebo impaired social working memory accuracy in participants with higher levels of social anxiety. No differences were found for non-social working memory or for AVP vs placebo. Results suggest that OT administration in individuals with higher levels of social anxiety may impair social cognitive functioning. Randomized-controlled trial registration: NCT01680718.

Interaction of CD38 variant and chronic interpersonal stress prospectively predicts social anxiety and depression symptoms over 6 years

Variation in the CD38 gene, which regulates secretion of the neuropeptide oxytocin, has been associated with several social phenotypes. Specifically, rs3796863 A allele carriers have demonstrated increased social sensitivity. In 400 older adolescents, we used trait-state-occasion modeling to investigate how rs3796863 genotype, baseline ratings of chronic interpersonal stress, and their gene–environment (G×E) interaction predicted trait social anxiety and depression symptoms over 6 years. We found significant G×E effects for CD38 A-carrier genotypes and chronic interpersonal stress at baseline predicting greater social anxiety and depression symptoms. A significant G×E effect of smaller magnitude was also found for C/C genotype and chronic interpersonal stress predicting greater depression; however, this effect was small compared with the main effect of chronic interpersonal stress. Thus, in the context of chronic interpersonal stress, heightened social sensitivity associated with the rs3796863 A allele may prospectively predict risk for social anxiety and (to a lesser extent) depression.