Neurobiology of mother–infant interactions: experience and central nervous system plasticity across development and generations

Abstract

The optimal coordination between the new mammalian mother and her young involves a sequence of behaviors on the part of each that ensures that the young will be adequately cared for and show healthy physical, emotional, and social development. This coordination is accomplished by each member of the relationship having the appropriate sensitivities and responses to cues that characterize the other. Among many mammalian species, new mothers are attracted to their infants’ odors and some recognize them based on their odors; they also respond to their infants’ vocalizations, thermal properties, and touch qualities. Together these cues ensure that the mother will nurse and protect the offspring and provide them with the appropriate physical and stimulus environment in which to develop. The young, in turn, orient to the mother and show a suckling pattern that reflects a sensitivity to the mothers odor, touch, and temperature characteristics. This article explores the sensory, endocrine, and neural mechanisms that underlie this early mother–young relationship, from the perspective of, first, the mother and, then, the young, noting the parallels between them. It emphasizes the importance of learning and plasticity in the formation and maintenance of the mother–young relationship and mediation of these experience effects by the brain and its neurochemistry. Finally, it discusses ways in which the infants’ early experiences with their mothers (or the absence of these experiences) may come to influence how they respond to their own infants when they grow up, providing a psychobiological mechanism for the inter-generational transmission of parenting styles and responsiveness.

Introduction

Non-human mammalian mothers typically display a stereotyped set of behavioral responses to their newborn. They exhibit species-characteristic ways of transporting, holding, feeding, and grooming the young, and of protecting them from the predators and other dangers [1]. For instance, the prospective mother rat constructs a nest before giving birth. She aids the birth by pulling individual pups from the vaginal canal, severs the umbilicus, eats the placenta, cleans the pups, and carries them one-by-one in her mouth to the nest. In the nest, she continues to lick the pups, especially their anogenital regions, and eventually adopts a nursing posture over them. In return, mammalian neonates exhibit behavior that is even more stereotyped and rigid than maternal behavior. This includes orchestrated orienting responses towards the mother, seeking and attachment to her teats, and emission of sound and odor signals that elicit maternal responses (crying, squealing, urination, and so forth). The reciprocal exhibition of maternal behaviors and newborn signaling promotes physiological and immunological resilience, physical maturation, and species-typical social and emotional development in the young (see [2], [3], [4], [5], [6], [7], [8]). Ultimately, reciprocal mother–infant behaviors increase the probability that the young will survive and, beyond survival, will mate and successfully rear their own offspring. In this article, we show how these behavior patterns, previously viewed as fixed and stereotyped, are in fact quite plastic, and depend on brain structure and function that was substantially influenced by experience at the time of birth and over the life-span.

As shown in Fig. 1, the development of the capacity to both express and modify maternal behavior patterns in adulthood may depend on mechanisms that were themselves activated and later tuned by early experiences. The interaction between the newborn and the mother alters basic mechanisms of behavioral expression in both. How the mother responds determines, in part, how the neurobiological and behavioral changes in the infant proceeds. Changes in an infant may eventually play out as to how the individual will respond to the offspring as an adult, and so on.