The neuroendocrinology of primate maternal behavior

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Abstract

In nonhuman primates and humans, similar to other mammals, hormones are not strictly necessary for the expression of maternal behavior, but nevertheless influence variation in maternal responsiveness and parental behavior both within and between individuals. A growing number of correlational and experimental studies have indicated that high circulating estrogen concentrations during pregnancy increase maternal motivation and responsiveness to infant stimuli, while effects of prepartum or postpartum estrogens and progestogens on maternal behavior are less clear. Prolactin is thought to play a role in promoting paternal and alloparental care in primates, but little is known about the relationship between this hormone and maternal behavior. High circulating cortisol levels appear to enhance arousal and responsiveness to infant stimuli in young, relatively inexperienced female primates, but interfere with the expression of maternal behavior in older and more experienced mothers. Among neuropeptides and neurotransmitters, preliminary evidence indicates that oxytocin and endogenous opioids affect maternal attachment to infants, including maintenance of contact, grooming, and responses to separation. Brain serotonin affects anxiety and impulsivity, which in turn may affect maternal behaviors such as infant retrieval or rejection of infants' attempts to make contact with the mother. Although our understanding of the neuroendocrine correlates of primate maternal behavior has grown substantially in the last two decades, very little is known about the mechanisms underlying these effects, e.g., the extent to which these mechanisms may involve changes in perception, emotion, or cognition.

Research Highlights

►Recent studies indicate that primate maternal behavior can be modulated by hormones and neuropeptides. ►Estrogen and oxytocin appear to enhance maternal responsiveness in female primates. ►The opioids may affect attachment to infants, but the exact nature of this effect is not clear. ►Cortisol may enhance maternal responsiveness in inexperienced females, but may inhibit maternal behavior in more experienced mothers. ►Both high corticotropin-releasing hormone and low serotonin levels within the brain appear to inhibit maternal behavior in primates.

Introduction

The laboratory rat has traditionally been the animal model of choice for research on the neuroendocrinology of maternal behavior, as maternal behavior in this species is predictably elicited and easily quantified, and modern invasive techniques for the manipulation and measurement of neuroendocrine variables can be used in this species (e.g., Bridges, 1990). For similar reasons, and with the additional advantage of having a large brain, the sheep has also been a favorite animal model for research in this area (e.g., Keverne and Kendrick, 1994). Studies of the neural and endocrine regulation of maternal behavior in rats and sheep have produced largely converging findings, leading to generalizations concerning the regulation of maternal behavior in mammals (Pryce, 1992, Numan and Insel, 2003).

Until the mid- to late 1980s, virtually no research was conducted on the neuroendocrinology of maternal behavior in primates. In part, this absence of research reflected the belief that maternal behavior in nonhuman primates and humans is learned early in life and later reinforced by experience acquired through reproduction (e.g., Keverne, 1996). Experiments with rhesus monkeys (Macaca mulatta) conducted in the 1950s and 1960s showed that socially deprived females displayed neglectful or abusive parenting with their first offspring, suggesting that opportunities to observe maternal behavior exhibited by other individuals and direct experience with one's own mother were necessary for the acquisition and expression of competent maternal care (Harlow and Seay, 1966, Ruppenthal et al., 1976). The abnormal behavior of socially deprived monkeys, however, was more likely the result of brain alterations induced by traumatic early experience and highly artificial laboratory housing conditions than of learning deficits (Maestripieri and Carroll, 1998a). Since the notion that maternal behavior is learned was consistent with the behaviorist paradigm, which dominated research in psychology for many decades, the “learning” interpretation of social-deprivation experiments went unchallenged for many years. The complementary assumption that maternal behavior in nonhuman primates and humans was largely emancipated from hormonal and other biological influences also went unchallenged for a long time (e.g., Coe, 1990, Keverne, 1996).

Studies of monkeys and humans in the late 1980s and 1990s, however, began to provide evidence that although hormones are not necessary for the expression of primate maternal behavior, they nevertheless may influence it (Pryce et al., 1988, Pryce et al., 1993, Maestripieri and Wallen, 1995, Maestripieri and Zehr, 1998). This is similar to what occurs in rodents, in which virgin females can be induced to express maternal motivation and behavior simply through gradual and repeated exposure to pups, a process known as sensitization (Numan and Insel, 2003). Studies with nonhuman primates and humans conducted in the past two decades have shown that hormones can influence the motivation to interact with infants and the quality of parental behavior, not only in females, but in males as well.

Because primates are generally characterized by long lifespans, slow life histories, and long periods of immature development, experience with infants gathered during the juvenile period can play a more significant role in the acquisition of primate parenting skills than in animals with short lifespans such as many rodents (e.g., Pryce, 1996). Female primates typically produce one infant at a time, and rarely twins, and invest heavily in each offspring, compared to other animals. Maternal investment in primates involves not only nutritional investment but also transport, protection, and transfer of social skills that are crucial for survival and success in a complex social environment. The importance of maternal investment in primates and the high cost of replacing a lost infant are other evolutionary reasons why experience is expected to play an important role in the acquisition and refinement of mothering skills. The same reasons, however, may also explain why parental motivation and behavior are not fully emancipated from hormonal influences: it would be too risky to do so. For example, a female primate who, for some reason, missed the opportunity to acquire experience with infants during the juvenile period and, as a result, lacked the motivation or the skills to take care of her own offspring, would pay a very high price. Hormones (including prenatal hormonal exposure) and neuropeptides increase the likelihood that females are motivated to interact with infants, thus gaining opportunities for learning, and also to maintain close contact with newborn offspring and meet their basic needs. Hormone and neuropeptide differences between individuals, and hormone and neuropeptide changes across ages and reproductive conditions, also ensure that levels of maternal motivation and maternal behavior are tailored to stable individual characteristics and are expressed at appropriate times in one's lifespan.

In this review article, we first address some of the considerations and caveats that should be kept in mind when interpreting findings on the neuroendocrinology of primate maternal behavior. Next, we briefly describe general patterns of maternal behavior in primates, highlighting major similarities and differences among taxa. We then review and examine the evidence that each of the major hormones, neuropeptides, and neutrotransmitters that have been implicated in the regulation of maternal behavior in nonprimate mammals – gonadal steroids, lactogenic hormones, oxytocin, hypothalamic-pituitary-adrenal (HPA) axis hormones, endogenous opioids, and serotonin – influences maternal behavior in nonhuman primates and humans. We conclude with a brief summary and a discussion of future research directions.

Section snippets

Considerations and caveats

The growing number of studies on the neuroendocrinology of parental behavior in primates, including humans, has increased our understanding both of normative parenting within species and of variation among species and among individuals. Most studies to date, however, have been correlational and have been conducted with relatively non-invasive measures of endocrine function. Experimental studies manipulating hormonal or neuropeptide signaling or investigating the effects of hormones,

Maternal behavior in primates

Maternal behavior can be defined broadly as any pattern of a mother's behavior that appears to enhance her offspring's survival and reproductive success. Interspecific differences in patterns of maternal behavior in primates are generally associated with differences in life styles and life histories, and in social, mating, and reproductive systems. Many species of prosimians are small-bodied, nocturnal, and solitary; in these species, infants are often parked in a nest while the mother is

Estrogens and progestogens

A common motif in behavioral endocrinology is the coordinated regulation by particular hormones of both specific physiological processes and the behaviors associated with those processes, with hormones exerting complementary effects in the periphery and in the brain. For example, aldosterone acts both on the kidneys to increase sodium reabsorption and in the brain to stimulate sodium ingestion, while androgens act on the testes and male reproductive tract to promote fertility and reproductive

Prolactin and placental lactogen

Prolactin is a protein hormone secreted by the anterior pituitary gland into the general circulation. In addition to its best-known function, stimulation of lactation, prolactin has numerous physiological and behavioral effects, including roles in metabolism, growth, and, in some taxa, parental behavior (Ben-Jonathan et al., 2008). Prolactin is able to cross the blood–brain barrier via a receptor-mediated transport mechanism in the choroid plexus, thereby entering the CSF and, presumably,

Oxytocin

Oxytocin is a nonapeptide synthesized primarily in two hypothalamic nuclei, the paraventricular nucleus (PVN) and the supraoptic nucleus (SON). Magnocellular oxytocinergic neurons from these nuclei project to the posterior pituitary, where oxytocin is stored in axon terminals and subsequently secreted into the general circulation. The major physiological functions of this neuropeptide are stimulation of myometrial contractions during parturition and stimulation of milk letdown during lactation;

Hypothalamic-pituitary-adrenal axis hormones

Stress, both chronic and acute, is thought to interfere with maternal behavior in primates. In nonhuman primates, anxiety and psychosocial or environmental stressors, such as crowding, receipt of aggression, and lack of social support, can increase the risk of infant abuse (Reite and Caine, 1983, Troisi and D'Amato, 1994, Maestripieri, 1994, Maestripieri and Carroll, 1998a, Maestripieri and Carroll, 1998b). In women, similarly, such stressors as poverty, domestic violence, sexual assault,

Endogenous opioids

The endogenous opioid peptides, including the endorphins, enkephalins, dynorphins, and endomorphins, are released both peripherally from the pituitary and centrally within a number of brain regions (Van Ree et al., 2000, Numan and Insel, 2003). Reproduction-related changes in opioids and their receptors have not been well characterized in primates, but plasma β-endorphin concentrations in women have been reported to be low during pregnancy and high during labor and the early postpartum period,

Serotonin

Serotonin is a monoamine neurotransmitter released by neurons that originate in the brainstem raphe nuclei and project to numerous brain regions (Lechin et al., 2006). The brain serotonergic system plays an important role in impulse control and in reducing the probability that risky, dangerous, or aggressive behaviors will be expressed in response to internal or external stimuli (e.g. Higley, 2003, Maestripieri, 2008a). Although serotonin is an obvious candidate neurotransmitter for the

Summary and conclusions

The last two decades have witnessed an enormous increase in the number of studies investigating the endocrinology and neurobiology of maternal behavior in human and nonhuman primates. All but a handful of these studies have been correlational, however, and effects of specific hormones, neuropeptides, and neurotransmitters on the expression of primate maternal behavior have rarely been investigated systematically across doses, contexts, or reproductive conditions. Thus, very few firm conclusions

Acknowledgments

Our studies of primate maternal behavior, some of which are reviewed here, were funded by grants NSF IBN-9604321 and NIH R21MH075973 (WS) and by NIH grants R03MH56328, R01MH57249, K02MH63097, and R21AG029862 (DM). We gratefully acknowledge the many colleagues, students, and technicians who contributed to this work, as well as the staff of the Larry Jacobsen Library of the National Primate Research Center at the University of Wisconsin-Madison for assistance with references. We also thank two

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