Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans

Abstract

The neuropeptide oxytocin enhances the processing of positive social stimuli and improves the capacity to effectively attend the eye region of conspecifics. To investigate the neural basis of these effects, we combined intranasal oxytocin administration with high-resolution functional magnetic resonance imaging in a unique emotion classification task. Emotional faces were briefly presented while controlling for the initial fixation, and measuring subsequent eye movements. Oxytocin had differential effects on the activity of specific amygdala subregions. On the one hand, it attenuated activation in lateral and dorsal regions of the anterior amygdala for fearful faces but enhanced activity for happy expressions, thus indicating a shift of the processing focus toward positive social stimuli. On the other hand, oxytocin increased the likelihood of reflexive gaze shifts toward the eye region irrespective of the depicted emotional expression. This gazing pattern was related to an increase of activity in the posterior amygdala and an enhanced functional coupling of this region to the superior colliculi. Thus, different behavioral effects of oxytocin seem to be closely related its specific modulatory influence on subregions within the human amygdala.

Intranasal Oxytocin Administration Dampens Amygdala Reactivity towards Emotional Faces in Male and Female PTSD Patients

“…Notably, OT administration effects were lateralized to the left amygdala, although the same (albeit non-significant) directionality of effects was observed in the right amygdala. In line with our findings, OT administration effects in left amygdala reactivity toward emotional faces have been found in healthy males (Gamer et al, 2010;Kirsch et al, 2005), healthy females (Domes et al, 2010) and male patients with Asperger's syndrome (Domes et al, 2014). On the other hand, OT administration effects on right-sided amygdala reactivity toward emotional faces has also been observed in healthy males (Domes et al, 2007;Petrovic et al, 2008), females with and without BPD (Bertsch et al, 2013) and males with Asperger's syndrome (Domes et al, 2013).…”

“…Although OT administration has predominantly been found to dampen amygdala reactivity (eg, Domes et al, 2007;Kirsch et al, 2005;Petrovic et al, 2008), increased amygdala reactivity has also been observed after OT administration. OT administration resulted in enhanced amygdala reactivity toward happy faces in healthy males (Gamer et al, 2010), and toward fearful (Domes et al, 2010) and angry faces (Bertsch et al, 2013) and threatening scenes (Lischke et al, 2012) in healthy females. In addition, increased amygdala reactivity toward neutral faces was observed after OT administration in male patients with Asperger's syndrome (Domes et al, 2013(Domes et al, , 2014.…”

Amygdala–Hippocampal Connectivity Changes During Acute Psychosocial Stress: Joint Effect of Early Life Stress and Oxytocin

“…The sequence of OXT and PLA sessions was counter-balanced across subjects. We adopted a standardized protocol used in previous studies (Gamer et al, 2010;Labuschagne et al, 2010) where participants selfadministered a single intranasal dose of 24 IU OXT/PLA (three puffs per nostril, each puff with 4 IU, or 6.82 mg) under the supervision of the experimenter 45 min before each fMRI scanning session. Participants abstained from alcohol during the 24 h and from exercise, caffeine, and food for 1 h before the experiment.…”

Oxytocin blunts social vigilance in the rhesus macaque

“…Inhaled OT increases gaze toward the eye region of faces in humans (8,10,11) and increases the frequency and duration that rhesus macaques look at other monkeys (4). However, OT may not generally enhance social attention, but instead may bias social attention.…”

“…One possible mechanistic explanation for these complex effects is that OT may alter social attention, which would necessarily adjust the information available for social perception and decision making (4,5,(8)(9)(10). Inhaled OT increases gaze toward the eye region of faces in humans (8,10,11) and increases the frequency and duration that rhesus macaques look at other monkeys (4).…”