The biology of mammalian parenting and its effect on offspring social development

Abstract

Parents know the transformative nature of having and caring for a child. Among many mammals, giving birth leads from an aversion to infant stimuli to irresistible attraction. Here, we review the biological mechanisms governing this shift in parental motivation in mammals. Estrogen and progesterone prepare the uterus for embryo implantation and placental development. Prolactin stimulates milk production, whereas oxytocin initiates labor and triggers milk ejection during nursing. These same molecules, interacting with dopamine, also activate specific neural pathways to motivate parents to nurture, bond with, and protect their offspring. Parenting in turn shapes the neural development of the infant social brain. Recent work suggests that many of the principles governing parental behavior and its effect on infant development are conserved from rodent to humans.

Fig. 1. Giving birth in mammals leads to a transformation in maternal responsiveness toward infants

In rats (A), this includes increases in nest building, pup retrieval, nursing, and defense of pups. Although many rodent mothers will care for any pup they encounter, sheep (B) develop selective bonds with their own lambs and reject lambs that are not their own. Experimental research using rodents and sheep have revealed some of the hormonal and neural mechanisms responsible for the onset of maternal behavior. (A) Photo courtesy of Doris Bayerl and Oliver Bosch.

Fig. 2. Schematic illustrating the hormonal and neural synchronization of reproductive physiology and maternal behavior in rodents

Estrogen (E) and progesterone (P) secreted by the ovaries prepare the uterus for embryonic implantation, support placental development, and sensitize the MPOA to respond to oxytocin (OT) and prolactin (PRL). Prolactin released from anterior pituitary (AP) stimulates milk production in the mammary glands. Oxytocin released from the posterior pituitary (PP) stimulates uterine contractions during labor and milk letdown during nursing. OT, PRL, and dopamine (DA) signaling in the brain modulates communication between several neural pathways to initiate the onset of maternal behavior. GLU, glutamate; NAcc, nucleus accumbens; AMY, amygdala; PVN, paraventricular nucleus of the hypothalamus; VP, ventral pallidum; Thal, thalamus.

Fig. 3. Paternal brain function in humans revealed by fMRI

(A) The VTA in fathers is activated to a greater extent when viewing pictures of their own children compared with pictures of unknown adults. (B) The anterior insula in fathers is activated to a greater extent when listening to infant-cry stimuli compared with an auditory control tone. AC, auditory cortex.

Fig. 4. Relationship between testes volume and VTA fMRI signal in fathers in response to viewing pictures of their own children

(A) Structural MRI was used to estimate testicular volume in fathers. (B) VTA activation in fathers while viewing pictures of their own children is negatively correlated with testicular volume, controlling for both height and testosterone level. Adapted from (4).

Fig. 5. Postulated mechanisms supporting the intergenerational transmission of secure attachment in humans

Securely attached parents have higher baseline oxytocin (OT) and a more pronounced OT response to interactions with their children. OT augments the mesolimbic DA system response to visual child stimuli, enhancing their reward value. It also inhibits AMY and augments anterior insula (AI) responses to infant-cry stimuli, facilitating a more empathic reaction. OTmay also modulate prefrontal cortex activity to suppress negative emotional reactions to infant crying. These neurobiological influences promote responsive, affectionate caregiving, which in turn promotes OT activity in children, along with child attachment behaviors that further engage parental brain systems, resulting in a positive feedback cycle that culminates in a mentally healthy, securely attached child. Genetic influences of the child can also either support or interfere with child attachment behaviors and parent-offspring bonding. OFC, orbitofrontal cortex; PFC, prefrontal cortex.