Facilitation of social attraction and bonding by the evolutionarily conserved neuropeptide oxytocin is well-established in female mammals. However, accumulating behavioral evidence suggests that oxytocin may have evolved sex-specific functional roles in the domain of human social cognition. A critical question is how oxytocin differentially modulates neural processing of social information in men and women, leading to divergent behavioral responses. Here we show that intranasal oxytocin treatment produces sex-and valence-dependent increases in amygdala activation when women view individuals identified as praising others but in men those who criticize them. Women subsequently show increased liking for the faces of these individuals, whereas in men it is reduced. Thus, oxytocin may act differentially via the amygdala to enhance the salience of positive social attributes in women but negative ones in men. We hypothesize that oxytocin may have evolved different but complementary roles to help ensure successful reproduction by encouraging mothers to promote a prosocial rearing environment for offspring and fathers to protect against antisocial influences.T he hypothalamic neuropeptide oxytocin (OXT) plays a key role in promoting maternal behavior and mother-infant bonding in mammals (1) as well as pair bonds with males in monogamous species (2). Recent studies in both monkeys and humans have suggested that it has not only evolved a more extensive role in social cognition in female primates but also become progressively used by males in this domain (3). Although OXT appears to facilitate both salience and motivational aspects of social cues in both sexes (3, 4), there is increasing evidence that it may often produce opposite effects in these domains in men and women (5-7), raising the intriguing possibility that it has evolved some sex-specific functions at both neural and behavioral levels. In particular, behavioral studies have reported that whereas OXT tends to facilitate positive social judgments (7), social approach (8), kinship recognition (5), and altruism (9) in women, in men it can facilitate negative social judgments (7), social avoidance (10), competitor recognition (5), and selfishness (9). Similarly, in response to couple conflict, OXT decreased sympathetic activity and arousal in women but increased them in men (6). The neural basis of these opposing sex-dependent behavioral effects of OXT has not, however, been established.Previous research has shown that the amygdala has different responses to positive and negative valence social information in men and women (11) and also may be a critical target for sex-specific functional effects of OXT. The amygdala has a sexually dimorphic distribution and expression of OXT receptors in nonprimate mammals (12, 13), and separate OXT-application studies in humans have indicated that there may be differential amygdala reactivity to fearful faces and fearful/threatening scenes in men (14, 15) and women (16,17). Importantly, this region plays a key role in processing so...
In male Caucasian subjects, learning is facilitated by receipt of social compared with non-social feedback, and the neuropeptide oxytocin (OXT) facilitates this effect. In this study, we have first shown a cultural difference in that male Chinese subjects actually perform significantly worse in the same reinforcement associated learning task with social (emotional faces) compared with non-social feedback. Nevertheless, in two independent double-blind placebo (PLC) controlled between-subject design experiments we found OXT still selectively facilitated learning with social feedback. Similar to Caucasian subjects this OXT effect was strongest with feedback using female rather than male faces. One experiment performed in conjunction with functional magnetic resonance imaging showed that during the response, but not feedback phase of the task, OXT selectively increased activity in the amygdala, hippocampus, parahippocampal gyrus and putamen during the social feedback condition, and functional connectivity between the amygdala and insula and caudate. Therefore, OXT may be increasing the salience and reward value of anticipated social feedback. In the PLC group, response times and state anxiety scores during social feedback were associated with signal changes in these same regions but not in the OXT group. OXT may therefore have also facilitated learning by reducing anxiety in the social feedback condition. Overall our results provide the first evidence for cultural differences in social facilitation of learning per se, but a similar selective enhancement of learning with social feedback under OXT. This effect of OXT may be associated with enhanced responses and functional connectivity in emotional memory and reward processing regions.
Musicians undergoing long-term musical training show improved emotional and cognitive function, which suggests the presence of neuroplasticity. The structural and functional impacts of the human brain have been observed in musicians. In this study, we used data-driven functional connectivity analysis to map local and distant functional connectivity in resting-state functional magnetic resonance imaging data from 28 professional musicians and 28 nonmusicians. Compared with nonmusicians, musicians exhibited significantly greater local functional connectivity density in 10 regions, including the bilateral dorsal anterior cingulate cortex, anterior insula, and anterior temporoparietal junction. A distant functional connectivity analysis demonstrated that most of these regions were included in salience system, which is associated with high-level cognitive control and fundamental attentional process. Additionally, musicians had significantly greater functional integration in this system, especially for connections to the left insula. Increased functional connectivity between the left insula and right temporoparietal junction may be a response to long-term musical training. Our findings indicate that the improvement of salience network is involved in musical training. The salience system may represent a new avenue for exploration regarding the underlying foundations of enhanced higher-level cognitive processes in musicians.
Research into language-emotion interactions has revealed intriguing cognitive inhibition effects by emotionally negative words in bilinguals. Here, we turn to the domain of human risk taking and show that the experience of positive recency in games of chance-the "hot hand" effect-is diminished when game outcomes are provided in a second language rather than the native language. We engaged late Chinese-English bilinguals with "play" or "leave" decisions upon presentation of equal-odds bets while manipulating language of feedback and outcome value. When positive game outcomes were presented in their second language, English, participants subsequently took significantly fewer gambles and responded slower compared with the trials in which equivalent feedback was provided in Chinese, their native language. Positive feedback was identified as driving the cross-language difference in preference for risk over certainty: feedback for previous winning outcomes presented in Chinese increased subsequent risk taking, whereas in the English context no such effect was observed. Complementing this behavioral effect, event-related brain potentials elicited by feedback words showed an amplified response to Chinese relative to English in the feedback-related negativity window, indicating a stronger impact in the native than in the second language. We also observed a main effect of language on P300 amplitude and found it correlated with the cross-language difference in risk selections, suggesting that the greater the difference in attention between languages, the greater the difference in risk-taking behavior. These results provide evidence that the hot hand effect is at least attenuated when an individual operates in a non-native language.
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