Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors

Naturally occurring variations in maternal licking/grooming influence neura l development and are transmitted from mother to female offspring. We found that the induction of maternal behavior in virgin females through constant exposure to pups (pup sensitization) was significantly shorter in the offs pring of High compared with Low licking/grooming mothers, suggesting differ ences in maternal responsivity. In randomly selected females screened for i ndividual differences in maternal responsivity and subsequently mated, ther e was a significant and negative correlation (r = -0.73) between the latenc y to exhibit maternal behavior in the pup sensitization paradigm and the fr equency of pup licking/grooming during lactation. Females that were more ma ternally responsive to pups and that showed increased levels of pup licking /grooming also showed significantly higher oxytocin receptor levels in the medial preoptic area, the lateral septum, the central nucleus (n.) of the a mygdala, the paraventricular n. of the hypothalamus, and the bed n. of the stria terminalis. Intracerebroventricular administration of an oxytocin rec eptor antagonist to mothers on postpartum day 3 completely eliminated the d ifferences in pup licking/grooming, suggesting that differences in oxytocin receptor levels are functionally related to maternal behavior. Finally, es trogen treatment of virgin females significantly increased oxytocin recepto r binding in the medial preoptic area and lateral septum of female offsprin g of High, but not Low, licking/grooming mothers. These findings suggest th at maternal licking/grooming influences the development of estrogen sensiti vity in brain regions that regulate maternal behavior, providing a potentia l mechanism for the intergenerational transmission of individual difference s in maternal behavior.