Oxytocin selectively facilitates learning with social feedback and increases activity and functional connectivity in emotional memory and reward processing regions

Abstract

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.

How individual needs influence motivation effects: a neuroscientific study on McClelland’s need theory

“…Kohls et al (2013), for instance, found activations in the putamen and thalamus when social approval was anticipated, whereas Smith et al (2010) reported activations in these two brain areas when research participants felt rewarded after looking at attractive faces. Parallel to our findings, Hu et al (2015) recently showed that activations in both the putamen and the thalamus occurred when individuals were rewarded by a smile from another person. Additionally, Pfeiffer et al (2014) reported that putamen and thalamus activations were found when participants interacted with another person in an experiment, while these activations were not found when participants interacted with a computer.…”

Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles

“…These analyses reveal an increase in correlated Fos expression across PBN nuclei in aCSF-treated subjects relative to both unexposed controls and OTA-treated subjects, consistent with the hypothesis that central OTR signaling during sociosexual interaction and mating with a female enhances functional connectivity across the PBN in male prairie voles. These data are interesting in light of recent human fMRI studies showing that intranasal OT administration increases functional connectivity across a variety of striatal and limbic nuclei during various social contexts (Fan et al, 2015; Gorka et al, 2015; Hu et al, 2015; Riem et al, 2012); however, studies using intranasal OT should be interpreted with caution (Walum et al, 2015). …”

Oxytocin blurs the self-other distinction during trait judgments and reduces medial prefrontal cortex responses

“…Several studies have reported OXT effects on DMN regions associated with self‐processing, including increased activation in both the ACC and precuneus during self‐processing of disgust and in the insula for both self and other processing [Scheele et al, ]. Other studies have also reported OXT effects on functional connectivity involving the insula [Hu et al, ' Striepens et al, ] and mPFC [Sripada et al, ], although this has not been investigated in the context of self‐processing. In another event related potential study, OXT was found to decrease the differential amplitudes of a frontocentral positivity at 220 to 280 ms (P200) in the area of the mPFC and ACC during self‐ vs. valence‐judgments (self‐referential processing) [Liu et al, ].…”