Oxytocin enhances basolateral amygdala activation and functional connectivity while processing emotional faces: preliminary findings in autistic vs non-autistic women

Abstract

Oxytocin is hypothesized to promote social interactions by enhancing the salience of social stimuli. While previous neuroimaging studies have reported that oxytocin enhances amygdala activation to face stimuli in autistic men, effects in autistic women remain unclear. In this study, the influence of intranasal oxytocin on activation and functional connectivity of the basolateral amygdala-the brain's 'salience detector'-while processing emotional faces vs shapes was tested in 16 autistic and 21 non-autistic women by functional magnetic resonance imaging in a placebo-controlled, within-subject, cross-over design. In the placebo condition, minimal activation differences were observed between autistic and non-autistic women. However, significant drug × group interactions were observed for both basolateral amygdala activation and functional connectivity. Oxytocin increased left basolateral amygdala activation among autistic women (35-voxel cluster, Montreal Neurological Institute (MNI) coordinates of peak voxel = -22 -10 -28; mean change = +0.079%, t = 3.159, PTukey = 0.0166) but not among non-autistic women (mean change = +0.003%, t = 0.153, PTukey = 0.999). Furthermore, oxytocin increased functional connectivity of the right basolateral amygdala with brain regions associated with socio-emotional information processing in autistic women, but not in non-autistic women, attenuating group differences in the placebo condition. Taken together, these findings extend evidence of oxytocin's effects on the amygdala to specifically include autistic women and specify the subregion of the effect.

Keywords: autism; basolateral amygdala; emotional face processing; oxytocin; salience.

Fig. 1.

Boxplots showing median response time (in ms) for face-matching and shape-matching trials between groups (autistic vs non-autistic) and drug conditions (placebo vs oxytocin). Only the effect of task (matching faces vs shapes) was significant. **P < 0.01.

Fig. 2.

Boxplots showing activation of the left basolateral amygdala cluster identified in the group analysis (35 voxels, peak activation = −22 −10 −28) between drug conditions and groups. Each dot represents one participant and the gray lines connect their activation values for the contrast Faces > Shapes between drug conditions. Image is shown such that the left side is the left hemisphere. *P < 0.05.

Fig. 3.

Effects of oxytocin (vs placebo) on functional connectivity. Using the right basolateral amygdala as the seed, oxytocin increased connectivity with temporal lobe and occipital lobe clusters. A significant Drug × Group interaction was also observed such that oxytocin significantly increased connectivity with frontal lobe regions and the cerebellum among autistic women. All tests Z > 2.3, P < 0.05 cluster-corrected. Image is shown such that the left side is the left hemisphere.