Oxytocin Enhances Amygdala-Dependent, Socially Reinforced Learning and Emotional Empathy in Humans

Abstract

Oxytocin (OT) is becoming increasingly established as a prosocial neuropeptide in humans with therapeutic potential in treatment of social, cognitive, and mood disorders. However, the potential of OT as a general facilitator of human learning and empathy is unclear. The current double-blind experiments on healthy adult male volunteers investigated first whether treatment with intranasal OT enhanced learning performance on a feedback-guided item-category association task where either social (smiling and angry faces) or nonsocial (green and red lights) reinforcers were used, and second whether it increased either cognitive or emotional empathy measured by the Multifaceted Empathy Test. Further experiments investigated whether OT-sensitive behavioral components required a normal functional amygdala. Results in control groups showed that learning performance was improved when social rather than nonsocial reinforcement was used. Intranasal OT potentiated this social reinforcement advantage and greatly increased emotional, but not cognitive, empathy in response to both positive and negative valence stimuli. Interestingly, after OT treatment, emotional empathy responses in men were raised to levels similar to those found in untreated women. Two patients with selective bilateral damage to the amygdala (monozygotic twins with congenital Urbach-Wiethe disease) were impaired on both OT-sensitive aspects of these learning and empathy tasks, but performed normally on nonsocially reinforced learning and cognitive empathy. Overall these findings provide the first demonstration that OT can facilitate amygdala-dependent, socially reinforced learning and emotional empathy in men.

Oxytocin Facilitates Pavlovian Fear Learning in Males

“…As of yet, however, there has been no data-driven explanation as to why PTSD affects victims of various types of traumas at differential rates: intentional acts of interpersonal violence, in particular sexual assault, lead to PTSD at far higher rates than do accidents or disasters (Cantor, 2009). There is evidence at least in females that interpersonal stress is linked to heightened endogenous OXT release (Taylor et al, 2010), and we have previously shown that heightened OXT increases learning in a social context (Hurlemann et al, 2010). Taken together with the results of the current study, we speculate that vulnerability for SAD and socially elicited PTSD could be associated with OXT's enhanced adaptation to social situations as discussed above.…”

“…Furthermore, in accordance with previous findings (Rash et al, 2014), OXT attenuated both neural and psychophysiological responses to the aversive electric shock. Thus an OXT-induced augmentation of fear conditioning cannot be attributed to increased pain responses but appears to be mediated by improved learning (Hurlemann et al, 2010).…”

“…During this paradigm, neutral conditioned stimuli (CS+) were paired with an aversive, unconditioned stimulus (UCS) (electric shock) in 70% contingency, while other neutral stimuli were never paired with the UCS (CS-). To account for previous findings suggesting that OXT specifically modulates processing of social stimuli (Hurlemann et al, 2010;Scheele et al, 2012), we included a social CS pair (face CS+, face CS− ) and a non-social CS pair (house CS+, house CS− ). The fMRI conditioning procedure started 30 min after inhalation of the nasal spray.…”

Region-specific up-regulation of oxytocin receptor binding in the brain of mice following chronic nicotine administration

“…Since oxytocin is also considered as a key mediator of social cognition in humans [37] and this effect has been postulated to specifically involve the OT system in the Amy [38], the OTR upregulation observed here might also be associated with a possible nicotine regulation of cognition through an OTR-dependent mechanism. However, this hypothesis needs to be further investigated.…”

Pathologic Evaluation of the Supraoptic and Paraventricular Nuclei in Dementia

“…In animal models administration of oxytocin increases maternal behaviours including grooming, nesting, and pair bond formation [22][23][24] . In humans, administration of oxytocin to healthy adults increases trust and cooperative behaviours 25,26 , emotional empathy 27 , facial expression recognition [28][29][30] , and theory of mind skills 31 . In addition, oxytocin administration to autistic patients facilitates social information processing and decreases repetitive behaviours 32,33 .…”