Testosterone administration modulates neural responses to crying infants in young females

Abstract

Parental responsiveness to infant vocalizations is an essential mechanism to ensure parental care, and its importance is reflected in a specific neural substrate, the thalamocingulate circuit, which evolved through mammalian evolution subserving this responsiveness. Recent studies using functional Magnetic Resonance Imaging (fMRI) provide compelling evidence for a comparable mechanism in humans by showing thalamocingulate responses to infant crying. Furthermore, possibly acting on this common neural substrate, steroid hormones such as estradiol and testosterone, seem to mediate parental behavior both in humans and other animals. Estradiol unmistakably increases parental care, while data for testosterone are less unequivocal. In humans and several other animals, testosterone levels decrease both in mothers and fathers during parenthood. However, exogenous testosterone in mice seems to increase parenting, and infant crying leads to heightened testosterone levels in human males. Not only is the way in which testosterone is implicated in parental responsiveness unresolved, but the underlying mechanisms are fully unknown. Accordingly, using fMRI, we measured neural responses of 16 young women who were listening to crying infants in a double blind, placebo-controlled, counterbalanced, testosterone administration experiment. Crucially, heightened activation in the testosterone condition compared to placebo was shown in the thalamocingulate region, insula, and the cerebellum in response to crying. Our results by controlled hormonal manipulation confirm a role of the thalamocingulate circuit in infant cry perception. Furthermore, the data also suggest that exogenous testosterone, by itself or by way of its metabolite estradiol, in our group of young women acted on this thalamocinculate circuit to, provisionally, upregulate parental care.