Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers

Abstract

This study investigates paternal brain function with the hope of better understanding the neural basis for variation in caregiving involvement among men. The neuropeptides oxytocin (OT) and vasopressin (AVP) are implicated in paternal caregiving in humans and other species. In a double-blind, placebo-controlled, within-subject pharmaco-functional MRI experiment, we randomized 30 fathers of 1-2year old children to receive either 24IU intranasal OT before one scan and placebo before the other scan (n=15) or 20IU intranasal AVP before one scan and placebo before the other scan (n=15). Brain function was measured with fMRI as the fathers viewed pictures of their children, unknown children and unknown adults, and as they listened to unknown infant cry stimuli. Intranasal OT, but not AVP, significantly increased the BOLD fMRI response to viewing pictures of own children within the caudate nucleus, a target of midbrain dopamine projections, as well as the dorsal anterior cingulate (dACC) and visual cortex, suggesting that intranasal oxytocin augments activation in brain regions involved in reward, empathy and attention in human fathers. OT effects also varied as a function of order of administration such that when OT was given before placebo, it increased activation within several reward-related structures (substantia nigra, ventral tegmental area, putamen) more than when it was given after placebo. Neither OT nor AVP had significant main effects on the neural response to cries. Our findings suggest that the hormonal changes associated with the transition to fatherhood are likely to facilitate increased approach motivation and empathy for children, and call for future research that evaluates the potential of OT to normalize deficits in paternal motivation, as might be found among men suffering from post-partum depression.

Keywords: Father; Oxytocin; Vasopressin; fMRI.

Fig. 1

OT effects on the neural response to own child picture stimuli. a) Brain regions where OT augmented the contrast between viewing own children and adult picture stimuli (O-A), b) average percent signal change (±1 SE) within three functional ROIs from a). Adult happy (AH), adult neutral (AN), adult sad (AS), own happy (OH), own neutral (ON), own sad (OS), unknown happy (UH), unknown neutral (UN), unknown sad (US).

Fig. 2

OT effects on the BOLD response to viewing different facial expressions of emotion in own children. Brain areas in which OT augments the contrast a) own child neutral faces - adult neutral faces and b) own child happy faces - adult happy faces.

Fig. 3

Significant drug by order of administration (OT-PL vs. PL-OT) interaction. a) Brain regions where OT-PL group demonstrated a larger oxytocin effect than PL-OT group for own-adult contrast; b) plot of mean % signal change with ±1 SE error bars at each scan for both orders of administration. Note that the data are plotted such that main effects of OT would yield lines of differing slope, whereas interaction effects yield lines with similar slopes.