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Oxytocin: prosocial behavior, social salience, or approach-related behavior?

2010
Andrew Kemp
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CORRESPONDENCE Oxytocin: Prosocial Behavior, Social Salience, or tainty about the predictive value of social stimuli, which may Approach-Related Behavior? then facilitate approach behaviors. Shamay-Tsoory et al. (1,3) argue that their hypothesis relating to a more general effect of To the Editor: oxytocin on social salience reconciles the prevailing view that W e read with much interest the article by Shamay-Tsoory oxytocin increases prosocial behavior with contradictory and colleagues, which reported that oxytocin increases findings of increased aggression following administration of envy and gloating (1), and recent correspondence oxytocin (16). We note that the psychology and neuroscience debating whether oxytocin is engaged in positive prosocial of aggression has also conceptualized this behavior as ap- behavior (2) or increases the salience of social behaviors more proach-related (17). Importantly, the dimensional approach- generally (3). Shamay-Tsoory et al. (1) required participants to withdrawal model may be a better explanation for brain play a game of chance with another (fake participant) who either activation associated with different emotions than the valence won more money (envy manipulation), lost more money (gloat- (positive/negative) and arousal (high activation/low activa- ing manipulation), or won and lost equal amounts of money. The tion) model (18). authors concluded that oxytocin may provoke a wide range of In conclusion, the findings reported by Shamay-Tsoory are social behaviors including the negative social emotions, envy important in that they highlight the complexity of oxytocin- and gloating. Mattie Tops (2) argued, however, that the results mediated changes in social behavior. We highlight an alternative can be explained by oxytocin-induced increases in social en- interpretation of their findings such that oxytocin serves to gagement and perspective taking, rather than negative social increase approach-related behaviors, which may include nega- emotions, given that one of the envy-related emotion items (“I tive social emotions such as envy and gloating, while decreasing would like to be in the other person’s shoes”) was more affected withdrawal-related behaviors as suggested by neuroimaging by the administration of oxytocin than other items. We should studies that have focused on the impact of oxytocin on amygdala point out that although Shamay-Tsoory et al. state that oxytocin function. Future research should examine the impact of oxytocin does not increase envy when the participant gained more money more broadly and directly test the hypothesis that oxytocin than the other player (i.e., the relative gain condition, a condition increases approach-related behaviors while decreasing with- in which envy would not be expected to be elicited), the statistic drawal-related behaviors. for this finding actually bordered on significance (for envy ratings Andrew H. Kemp p ⫽ .051, but not for the envy index, p ⫽ .12). We suggest an additional alternative hypothesis not discussed in the commen- School of Psychology tary on Shamay-Tsoory et al. (1): that oxytocin may serve to University of Sydney increase approach-related behaviors while inhibiting with- Sydney, Australia drawal-related behaviors. E-mail: akemp@usyd.edu.au Approach and withdrawal behaviors are dimensions on which Adam J. Guastella affective processes may be organized (4 – 6). Approach behaviors Brain and Mind Research Institute are appetitive in nature, generally associated with positive affective University of Sydney states, and involve moving toward a desired goal (e.g., happiness, Sydney, Australia enthusiasm, trust). Withdrawal behaviors are considered aversive in nature and involve moving away from a source of negative stimu- The authors report no biomedical financial interests or po- lation (e.g., fear, disgust, anxiety). A key component of both tential conflicts of interest. approach and withdrawal behavior is motivation, and therefore relates to the organization of affect more generally (7,8). We distinguish between positive/negative social behaviors and ap- 1. Shamay-Tsoory SG, Fischer M, Dvash J, Harari H, Perach-Bloom N, Levkovitz Y (2009): Intranasal administration of oxytocin increases envy and Schaden- proach/withdrawal-related behaviors, such that whereas positive freude (gloating). Biol Psychiatry 66:864 – 870. social behaviors (or prosocial behaviors) are generally approach- 2. Tops M (in press): Oxytocin: Envy or engagement in others [published related, negative social behaviors may also be approach related online ahead of print Oct 21]? Biol Psychiatry. doi:10.1016/j. (e.g., envy and gloating). biopsych.2009.08.032. Research has recently highlighted the distinction between 3. Shamay-Tsoory SG (in press): One hormonal system for love and envy: A positive emotions and approach-related behaviors (9,10). For reply to Tops [published online ahead of print Oct 21]. Biol Psychiatry. doi:10.1016/j.biopsych.2009.09.002. example, although anger is a negative emotion, it is an 4. Cacioppo J, Gardner W (1999): Emotion. Annu Rev Psychol 50:191– approach-related behavior because it involves approaching a 214. particular desired outcome, which may involve the creation of 5. Davidson R (2003): Affective neuroscience and psychophysiology: To- discomfort for someone else or of rectifying an injustice (9). ward a synthesis. Psychophysiology 40:655– 665. Similarly, jealousy, an experience consistent with envy, is 6. Russell J (2003): Core affect and the psychological construction of emo- tion. Psychol Rev 110:145–172. correlated with anger (10) and belongs to the “family” of 7. Lang P, Bradley M, Cuthbert B (1998): Emotion, motivation, and approach-related emotions (11). Moreover, both jealousy (10) anxiety: Brain mechanisms and psychophysiology. Biol Psychiatry and anger (12) elicit left frontal cortical activation, a pattern of 44:1248 –1263. activation consistent with approach-related behaviors. Gloat- 8. Davidson R, Irwin W (1999): The functional neuroanatomy of emotion ing is the malicious pleasure at another’s misfortune (13) and and affective style. Trends Cogn Sci 3:11–21. is therefore related to happiness, an approach-related behav- 9. Carver C, Harmon-Jones E (2009): Anger is an approach-related affect: Evidence and implications. Psychol Bull 135:183–204. ior, albeit in a negative social context. Recent neuroimaging 10. Harmon-Jones E, Peterson C, Harris C (2009): Jealousy: Novel methods studies highlight that oxytocin reduces amygdala activation in and neural correlates. Emotion 9:113–117. response to fear-inducing stimuli (14) and emotional faces 11. Lazarus R (1991): Emotion and Adaptation. New York: Oxford University regardless of valence (15), suggesting reductions in uncer- Press. 0006-3223/10/$36.00 BIOL PSYCHIATRY 2010;67:e33– e34 © 2010 Society of Biological Psychiatry e34 BIOL PSYCHIATRY 2010;67:e33– e34 Correspondence 12. Harmon-Jones E, Allen J (1998): Anger and frontal brain activity: EEG 16. 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Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62:1187–1190. doi:10.1016/j.biopsych.2009.11.019 www.sobp.org/journal