Which maternal behavior is the nurse most likely to see when a new mother receives her infant for the first time?

1.12.3.5.3 Mechanisms – potential pathways

Maternal behavior includes both approach and avoidance. Nonparental animals avoid pups; parental animals approach and retrieve them. Based on lesion, tract tracing, and fos studies, Numan (2007) has proposed an elegant model for maternal behavior that encompasses both these aspects. First, aversive reactions to pup stimuli seem to be mediated by the olfactory system and the medial amygdala as outlined above. The medial amygdala sends projections to a number of hypothalamic nuclei involved in defensive reactions to aversive stimuli, including the AH and VMH (Canteras, 2002). Pheromonal stimulation of this nucleus is thought to increase the aversive aspects of pup stimuli.

Second, the appetitive aspects of maternal behavior (i.e., crouching and pup retrieval) are mediated by the vBNST via DA release. By combining fos immunolabeling with tract tracing, Numan and Numan (1997) have shown that neurons stimulated during the expression of maternal behavior maintain distinct projection targets. Those in the vBNST, not the mPOA, project to the VTA. Thus, it is likely that vBNST plays the greater role in the appetitive aspect of pup stimuli. Further, while the specific stimuli for appetitive maternal behavior are not known, it is tempting to speculate that chemosensory cues processed by the BNST induce this behavior.

DA has been proposed to increase motivation in a variety of behaviors by disinhibiting the ventral pallidum (VP) via the nucleus accumbens. Numan (2007) predicted that the same pathway was involved in DA regulation of maternal behavior. A recent study from his lab has confirmed and extended this hypothesis by showing that a D1 antagonist facilitates maternal behavior when injected into either the nucleus accumbens or the mPOA of pregnancy-terminated rats. This mechanism is only activated in the presence of the appropriate gonadal steroids. Thus, the final mechanism underlying steroidal regulation of maternal behavior resembles that of copulation.

Introduction

Maternal behavior emerges and wanes over the course of development in female mammals. In recent years, our understanding of the biochemical regulation of maternal care and the neural substrates involved in regulating the expression of maternal behavior has significantly increased. This article focuses primarily, but not exclusively, on research conducted in rodents, species that have provided a foundation for our understanding a complexity of processes associated with raising and nurturing young. The initial objective is to identify or define maternal behavior. The underlying physiological events that transpire during pregnancy and lactation are then presented in light of their roles in affecting maternal care. Next, the actions of the hormones of pregnancy on the neural substrates that regulate maternal responsiveness are discussed as well as the role of genetic and epigenetic factors and their interactions over the course of development. Finally, the effects of experience on the modification of parental care are explored. This article is not fully comprehensive; rather, it is designed to present a broad overview of the neuroendocrine and endocrine–neural regulation of maternal behavior.

A FACTORS THAT AFFECT THE DAM’S BEHAVIOR

The mother’s physiological condition at the time of giving birth is the first essential for a successful interaction.

Maternal behavior begins during the early stages of parturition. The ewe paws the ground, licking up the fetal fluids after the birth membranes have ruptured, and begins making soft, low-frequency “rumble”-type vocalizations (Shillito and Hoyland, 1971). When her lamb emerges in a pool of amniotic fluid she rises within about a minute (Bareham, 1976; Arnold and Morgan, 1975), turns to the lamb, and begins to lick it, at the same time sucking up and ingesting the fetal fluids and membranes.

The dam’s behavior has been rendered maternal by gonadal steroids (Poindron and LeNeindre, 1980) comparable with those acting during pregnancy in the rat (Rosenblatt and Siegel, 1983). However, Poindron et al. (1988) have shown that the full complement of her maternal behavior, defined as licking, low-pitched bleats, and acceptance at the udder, is not always elicited by hormonal priming alone. It is facilitated by the smell of fetal fluid (Levy et al., 1983), amniotic fluid from her own lamb being more powerfully attractive than that of an alien one (Levy and Poindron, 1984, 1987), and by the vaginal-cervical stimulation which occurs during labor and expulsion of the lamb (Keverne et al., 1983).

The ewe’s maternal behavior is also affected by previous experience. In primiparous animals it tends to develop more slowly after giving birth and is less certain. In the induction of maternal behaviour in nonpregnant animals, primiparous animals were found to be less responsive to hormones than multiparas (LeNeindre et al., 1979; Poindron and LeNeindre, 1980). Among pregnant ewes delivered by cesarian section, no primiparous animals showed maternal behavior within 3 days, whereas almost all multiparas did so, suggesting that the former require stimulation of the birth canal for a normal response to the lamb (Alexander et al., 1988). Also, unlike multiparas, amniotic fluid on the birth coat is necessary for primiparas to develop maternal behavior at parturition (Levy and Poindron, 1987). More recently, oxytocin has been implicated in the hormonal stimulation of the ewe’s maternal behavior (Kendrick et al., 1987), and Levy et al. (1992) have shown that vaginocervical stimulation, as the major factor facilitating a rapid onset of maternal behavior, acts via intracerebral oxytocin secretion in primiparous as well as multiparous parturient ewes.

The ewe’s maternal behavior gradually declines unless it is reinforced by the presence of a lamb. If the lamb is removed at birth and kept away for l–4 hr, many dams will still accept it, although the numbers that accept fall off with the time since separation (Poindron et al., 1979; Alexander et al., 1986). However, if her own lamb is removed at birth, the ewe will usually accept a newly bom alien lamb (Smith et al., 1966). Once she has licked her lamb for a few minutes she will butt away an alien (Herscher et al., 1963), although it takes 2–4 hr for ewes to become completely selective (Poindron et al., 1980); therefore learning her own lamb’s characteristics can modify, or direct, the ewe’s maternal behavior. This learning appears to be based on smell: Poindron (1976) has shown that the dam recognizes her lamb by its odor when it comes to suck, and Alexander and Stevens (1985) have demonstrated that this odor can be transferred to an alien lamb, ultimately making it acceptable, even at 2–3 days after birth. Its smell, although important, is not the only factor which makes a newborn lamb acceptable. Baldwin and Shillito (1974) found that anosmic Soay ewes accepted their lambs, although they failed to lick them sufficiently and did not form the usual exclusive relationship with them. At parturition the dam is also attracted by lambs which are warm (Lynch and Alexander, 1973), newly born, wet and lying down (Poindron et al., 1980), and bleating (Smith et al., 1966).

5.3 Stress and Glucocorticoid Modulation of Reproductive Behavior Via Endocannabinoid Actions

Maternal behavior improves the survival and well-being of the offspring, and thus is important for the success of the species. In rodents, maternal behaviors include nest building, licking, arched-back nursing, lactation, and maternal aggression. Two peptide hormones are crucial for lactation. Prolactin, secreted from the anterior pituitary, promotes milk production by stimulating the alveoli of the mammary glands to secrete milk. Oxytocin, synthesized by the magnocellular neurons in the PVN and SON, activates smooth muscle cells in the mammary glands to stimulate milk letdown. In addition to stimulating milk letdown, oxytocin has been found to play an important role in maternal behavior and social interactions through central actions of the neuropeptide (Bosch, Meddle, Beiderbeck, Douglas, & Neumann, 2005; Insel, 2010; Numan & Insel, 2003; Pedersen & Boccia, 2002). Central administration of oxytocin elicits complete maternal behavior in virgin rats (Pedersen, Ascher, Monroe, & Prange, 1982), while disruption of the PVN, where many of the OT neurons reside, prevents the activation of maternal behavior (Insel & Harbaugh, 1989). In addition, mothers that display high pup licking/grooming also show increased oxytocin expression in the medial preoptic area and PVN (Shahrokh, Zhang, Diorio, Gratton, & Meaney, 2010). In prairie voles, virgin females that display maternal behavior exhibit a higher oxytocin receptor density in the nucleus accumbens (Olazabal & Young, 2006), an important source of dopamine involved in the brain reward circuitry. These studies indicate that the activity of oxytocin neurons may be modulated by environmental factors to regulate maternal behavior.

Stress and elevated circulating glucocorticoid levels have significant effects on maternal behavior. In lactating rats, the synthetic glucocorticoid dexamethasone reduces maternal behavior in dams, as evidenced by an increased latency to build nesting and to retrieve the first pup, decreased pup weight gain, and reduced time spent in the arched-back nursing position and licking the pups (Vilela & Giusti-Paiva, 2011; Vilela, Ruginsk, de Melo, & Giusti-Paiva, 2013). In addition, dexamethasone treatment also reduced maternal aggression and increased maternal anxiety, evidenced respectively by an increased latency to attack a male intruder and an increase in anxiety-like behavior in the elevated plus maze and open field test (Vilela et al., 2013). Dexamethasone administration also reduced oxytocin and prolactin secretion during lactation (Vilela & Giusti-Paiva, 2011).

As discussed above, glucocorticoid administration reduced the parameters of maternal care in lactating females (Vilela & Giusti-Paiva, 2011; Vilela et al., 2013). However, pretreatment of the female with the CB1 receptor antagonist AM251 reversed the glucocorticoid-triggered reduction of maternal behavior (Vilela et al., 2013), suggesting that the glucocorticoid effect on maternal behavior is mediated by endocannabinoid release. To investigate the effect of glucocorticoids on synaptic inputs to oxytocin neurons, we recorded the excitatory and inhibitory synaptic currents in putative magnocellular neuroendocrine cells in the PVN and SON from male rats (Di, Malcher-Lopes, et al., 2005). We found that glucocorticoids significantly decreased excitatory synaptic inputs and increased inhibitory synaptic inputs to magnocellular neurons by the activation of an unknown membrane-associated glucocorticoid receptor. The rapid glucocorticoid effect was insensitive to classical type I and type II corticosteroid receptor antagonists, but was blocked by inhibiting postsynaptic G-protein activity, suggesting it acted via a postsynaptic G protein signaling mechanism and synthesis of a retrograde messenger. Glucocorticoids caused a significant increase in both AEA and 2-AG levels in hypothalamic slices, and the rapid modulation of excitatory synaptic inputs by dexamethasone was blocked by CB1 receptor antagonists/inverse agonists and mimicked and occluded by CB1 agonists. These results suggested that a glucocorticoid-induced retrograde release of eCB was responsible for the inhibitory effect of glucocorticoid on glutamatergic synaptic transmission. On the other hand, glucocorticoids facilitated GABAergic transmission by activating nitric oxide production at GABAergic synapses (Di, Maxson, Franco, & Tasker, 2009), resulting in an overall inhibitory effect on the activity of oxytocin neurons by glucocorticoids in adult male rats. Future studies are required to determine the mechanism of glucocorticoid modulation of oxytocin neurons in lactating females.

Glucocorticoids were also found to rapidly suppress reproductive clasping behavior in the male salamander (Taricha) by the activation of eCB signaling (Coddington, Lewis, Rose, & Moore, 2007). Acute confinement stress or corticosterone administration suppressed clasping behavior in male Taricha (Moore & Miller, 1984). The suppressive effect of glucocorticoid was rapid, taking place 5–7 min after systemic injection of corticosterone (Orchinik, Murray, & Moore, 1991). In addition, the firing activities of neurons in the rostromedial medulla that respond to sensory stimulation during courtship are rapidly inhibited by corticosterone (Rose, Marrs, & Moore, 1998; Rose, Moore, & Orchinik, 1993). Intraperitoneal injection of a CB1 receptor agonist caused a similar suppression of clasping behavior in male Taricha (Soderstrom, Leid, Moore, & Murray, 2000), and pretreatment with the CB1 receptor antagonist abolished the stress- and corticosterone-induced suppression of clasping behavior, suggesting that eCBs may mediate stress-induced suppression of reproductive behavior (Coddington et al., 2007). The corticosterone suppression of neuronal firing in response to cloacal stimulation was blocked by a CB1 receptor antagonist. These results together suggest that the rapid suppression of sexual behavior in Taricha by stress and glucocorticoid is mediated by eCB release.

Quality of Care

Maternal behavior plays a central role in attachment theory and research. Bowlby suggested that a caregiving system complementary to the attachment behavioral system is necessary for attachment relationships to develop. Further, based on her studies, Ainsworth concluded that it was not the quantity but the quality of care that mattered most in accounting for the different types of infant–mother relationships. Although she observed specific maternal behaviors during interactions with infants, Ainsworth conceptualized four categories of behavior to describe the overall features of maternal care: sensitivity–insensitivity, cooperation–interference, acceptance–rejection, and accessibility–ignoring. Because those categories of maternal behavior turned out to be highly intercorrelated, the overall quality of maternal care was subsumed under the label of sensitivity.

Sensitivity to an infant’s signals and communications refers to a mother’s ability to see things from the baby’s perspective; that is, a mother’s ability to perceive her baby’s signals, interpret them correctly, and respond to them appropriately and promptly. Cooperation–interference refers to a mother’s ability to respect her baby as a separate individual, to intervene in the baby’s activities in a skillful and collaborative manner so that the baby does not experience it as interfering. Acceptance–rejection refers to the balance between a mother’s positive and negative feelings about her baby, and the extent to which she is able to resolve those negative feelings. Accessibility–ignoring refers to a mother’s ability to notice and attend to her baby’s signals despite demands from other sources on her attention.

Maternal behavior shapes the experience of stress

Maternal behavior is fundamental to survival in altricial species. The role of the mother can extend beyond the basics of food, warmth, and shelter. For example, in rodents, the HPA axis is highly regulated by interactions between dam and pup, and various maternal behaviors serve to minimize the pup's glucocorticoid release in response to stressors during critical neonatal periods of brain development. Human babies are also less responsive to stress over the first year of life, and their HPA axis is also regulated by social interactions. Thus, it is thought that maternal dampening of the HPA axis serves to protect the young from the detrimental effects of glucocorticoids on brain development. Rodents are born comparatively more immature in terms of their brain development than are people, and regions of the rat hippocampus are still experiencing high rates of development during the neonatal period. Disrupting maternal behavior by separating dams from pups for extended periods over neonatal life can lead to maladaptive behavior in the pups later in life, not unlike the consequences in adulthood found for prenatal stress. Studies in non-human primates also show that either maternal separation or environmental stressors during gestation and infancy can affect how the offspring respond to stressors in later life. Such animals are more timid and fearful as adults, and are more likely to show signs of depression.

In contrast, brief daily periods of separation of pups from dams (approximately 15 to 20 minutes) over neonatal life lead to a number of positive effects on brain and behavioral development in comparison to pups that were never separated from the dams, or pups that were separated for lengthy periods (several hours). Pups that were briefly separated on a daily basis had lower levels of glucocorticoid release in response to a stressor as adults, and were able to turn off the release of glucocorticoids more efficiently when the stress experience was over. Such animals are also less anxious and fearful as adults. The reduced exposure to glucocorticoids over the course of their lives means that these animals age more successfully: they are less likely to have hippocampal damage and cognitive impairments with age than other animals. Michael Meaney and his colleagues at McGill University have shown that the long-lasting effects of brief maternal separation are due to slight variations in the quality of care a pup receives. When the separation is of short duration, the behavior of the dams changes and they lick and groom their pups more than dams that are left undisturbed with their pups. Individual differences in the amount of such maternal behaviors received by the pups influences how the pups will interact with their environment in adulthood and how their HPA axis will function. As a result, these animals are less likely to encounter the negative effects of glucocorticoids on the brain and body.

The results discussed above indicate that stress experiences and stress hormones should not necessarily be thought of as developmental teratogens, like alcohol or lead or pesticides, that distort development during critical windows of opportunity. The long-term effects of stress experiences cannot always be characterized as harmful or negative. Researchers have speculated as to why brain development is so susceptible to such early life experiences. For example, Martin Teicher of Harvard University has hypothesized that early stress experiences may prod brain development in an adaptive way, causing the nervous system to become more suited to its environment. Brain development may be routed toward greater vigilance and stress responsiveness in anticipation of a treacherous environment based on harsh early life experiences. On the other hand, brain development may be routed toward better stress-coping strategies when exposed to mild, short-lived stressors and appropriate nurturing. While this may be true in terms of selective pressures on various species in evolutionary history, the costs of severe deprivation and abusive life experiences in childhood on physical and mental health and on longevity suggest that there are limits to adaptation.

4.31.4.4 Maternal Behavior and Epigenetic Modifications

Maternal behavior has been shown to affect the epigenetic programming of offspring. In an elegant set of rat studies for example, it was demonstrated that the amount of licking and grooming performed by the mother influenced the methylation pattern of the GCR promoter in the offspring. Offspring from mothers that were high lickers and groomers (HLG) showed very little methylation in the hippocampal NGFI-A TRE found within exon 17 GCR promoter sequence, while offspring from mothers that were low lickers and groomers (LLG) showed methylation at the same site (Weaver et al., 2007, Weaver et al., 2004). As mentioned earlier, the exon 17 GCR promoter sequence in the hippocampus is an important regulator for terminating the stress response via the negative feedback loop. In rat pups born to LLGs, there was decreased binding of transcription factor NGFI-A to the GCR promoter and a subsequent increase in their stress response (Weaver et al., 2007). In contrast, offspring born to HLG mothers had a lower, more typical stress response as adults.

Nonhuman primate studies have also demonstrated that maternal behavior alters epigenetic programming of offspring. When nonhuman primates were completely deprived of maternal care, an increase in their HPAA response was observed during adulthood (Veenema, 2009). Likewise, an increased HPAA response and more fearful behavior were also observed in macaque offspring when their mothers were exposed to variable forage patterns during lactation (Rosenblum and Andrews, 1994). This alteration in the stress response was not observed in offspring whose mothers had access to either high or low foraging patterns, suggesting that the unpredictability of available nutrition plays a role in programming these responses (Rosenblum and Andrews, 1994). These studies are intriguing and suggest that variation in agriculture management practices could play an important role in shaping the stress response and overall well-being of the livestock animals. Animals that experience less stress are typically less prone to infection and disease experience better food to gain ratios and typically produce a higher-quality meat product.

Maternal care

Maternal behaviour in mammals is characterized by lactation. Via the milk, offspring are provided with nutrients, calories, vitamins, minerals, and passive immune protection (lymphocytes and antibodies), for growth and for metabolism [31, 92]. As a consequence, a long lactation period is beneficial for the pups. For the mother, on the other hand, the energetic costs of lactation may influence her survival and future reproduction. The metabolic demands of lactation are enormous, especially for small animals, and in house mice they are more than four times higher than the energetic costs of gestation [93]. Daily energy output in milk per unit body weight is approximately 16 times higher than in an animal the size of a cow [94]. Such high and sustained milk production in small mammals is only possible because of a high metabolic rate that also relates to a decrease in lifespan [95, 96]. In addition, the longer the lactation period, or the more milk produced, the more delayed is the birth of the next litter [33, 34]. As a consequence, lactating females have to make a trade-off between current and future reproduction, and we expect flexible maternal strategies to compromise between offspring benefits and maternal costs during lactation under different environmental conditions. The potential for rather flexible maternal strategies is already illustrated by the observation that reproductive performance varies among different inbred strains [91, 97].

Maternal behaviour in house mice consists of nursing, licking and grooming pups (licking the anogenital region stimulates defecation in pups), nest-building behaviour, huddling over pups to keep them warm (under conditions of low temperature) and retrieving pups to the nest, either when females move the nest to another place, or when a nursing mother has left the nest, and some pups were dragged along because they were still attached to a teat [31]. It is interesting to note that male house mice, when kept in a monogamous pair with a female, show the same parental behaviours as females towards their offspring, except for nursing [31].

House mice as well as laboratory mice build nests in which they sleep or rest. Such nests are often relatively small and open, but are more closely built during periods of cold environmental conditions [91]. Pregnant and lactating females, on the other hand, build maternal nests (from approximately 4 days after mating onwards) that are two to three times the size of a sleeping nest, with one or two entrances and completely enclosed. Maternal nests are an important component of maternal behaviour. When given the choice between different bedding materials, including an option with no bedding material present, female laboratory mice never gave birth in cages without bedding [98]. Under natural or semi-natural conditions, access to a safe and protected nesting site seems to be a prerequisite for successful reproduction in females, because such sites improve protection from disturbances by conspecifics [41, 99–101]. It is therefore highly recommended to provide mice with nest-building material in laboratory animal facilities.

Maternal aggression refers to aggressive behaviour of a lactating female when defending her litter [91]. Females become intensely aggressive towards other individuals during the final days of pregnancy and during lactation, and will vigorously protect their nest, biting intruders’ heads and bellies [102, 103]. Such increased aggression may function to allow the female to defend her nest and pups against infanticidal conspecifics (both male and female house mice have been observed to kill pups when encountered in a foreign nest), or assess the dominance status of any intruding males [104–106].

5.2.9 Changes in the Function of MPOA across the Postpartum Period

The maternal behavior of rats varies over the postpartum period [832]. Early in the postpartum period, up to day 10, pups that have been displaced from the nest are quickly retrieved and then nursed. During the mid-postpartum period (days 12–21), displaced pups are less likely to be retrieved, although nursing behavior remains high. Subsequently, nursing behavior also declines and weaning occurs by day 28 postpartum. A functional explanation of the decline in retrieval behavior after day 10 postpartum is that older pups are mobile enough to crawl to the nest area and do not require maternal transport. Therefore, young pups appear to activate retrieval while older pups do not. It is also interesting to note that if female rats are kept with young pups across the postpartum period (once a given litter reaches 10 days of age, it is replaced with a younger litter), they continue to show high levels of both retrieving and nursing for long periods of time [695].

Earlier in this chapter, I indicated that the MPOA is involved in both the appetitive and consummatory aspects of maternal behavior, since MPOA lesions depress both retrieving and nursing. Based on the course of maternal behavior over the postpartum period, as pups advance in age, one might conclude that young pups are able to activate both appetitive and consummatory MPOA mechanisms, older pups activate only consummatory processes, and even older pups activate neither mechanism, resulting in weaning.

In an interesting study, Pereira and Morrell [753] examined the effects of inactivation of the MPOA on the maternal behavior of female rats on either day 7 or day 14 postpartum. In order to inactivate the MPOA, they used local bupivacaine injections. Bupivacaine is similar to lidocaine and is a drug that blocks voltage-gated Na+ channels and therefore blocks the production of action potentials. This fact is relevant because it indicates that bupivacaine would not only block MPOA neuron activity but would also block the activity of axons passing through the MPOA (axons of passage), but having their origins (cell bodies) elsewhere. Pereira and Morrell reported that bupivacaine injections into the MPOA disrupted retrieval behavior in rats when the injections were performed on day 7 postpartum, but that the injections actually stimulated retrieval behavior when they were performed on day 14 postpartum, at a time when such females typically do not retrieve their mobile pups. Pereira and Morrell [753] proposed that the functional role of the MPOA with respect to maternal behavior changes over the course of the postpartum period (cf. [756]).

These results are difficult to interpret. It is possible that bupivacaine primarily inhibits those neurons that are most active at the time of its injection. If fibers of passage through the MPOA, with origins and terminations distinct from MPOA neurons, were most active in day 14 postpartum females, and if such activity served to inhibit retrieval behavior, then retrieval might have been facilitated in the late postpartum rats not because of the depression of MPOA neurons but because of depression of an inhibitory system whose axons pass through the MPOA. Therefore, the possibility that the direct inactivation of MPOA neurons in the mid-postpartum period increases appetitive maternal responses will need to be confirmed through the use of methods that are neuron (cell body) specific and do not disrupt axons of passage, such as lesion production with excitotoxic amino acids or neuropharmacological inactivation with agents such as muscimol and/or baclofen. That the results obtained with bupivacaine are questionable relates to the finding by Pereira and Morrell [753] that bupivicaine injections aimed at the lateral preoptic area and ventral pallidum did not interfere with maternal behavior during the early postpartum period, while it is well known that excitotoxic amino acid lesions and muscimol inactivation of these regions do disrupt maternal behavior in such females [701,708][701][708].

A related explanation of the Pereira and Morrell [753] results arises from a recent finding by Smith, Holschbach, Olsewicz, and Lonstein [913] that medullary norepinephrine (NE) input to the dorsal MPOA region serves to depress retrieval behavior in postpartum rats, presumably by inhibiting MPOA neurons. Perhaps such NE input to MPOA is normally active in day 14 postpartum females and operates to depress the retrieval of older pups. Further, bupivacaine may have acted to selectively depress such NE input, so that older pups could be retrieved. Therefore, it is premature to conclude that bupivacaine injections into MPOA stimulate a resumption of retrieval behavior in day 14 postpartum females as result of depressing the activity of MPOA neurons. The observed effects could have resulted from depressing the activity of axons of passage through the MPOA or from depressing the activity of particular types of afferent inputs to the MPOA region.

12.5 Hormones and Parental Behavior

While maternal behavior in vertebrates is strongly associated with prolactin, a peptide hormone produced in the anterior pituitary, in male vertebrates parental care is associated with declining levels of testosterone. In female birds, prolactin stimulates nesting behavior and operates, via positive feedback, to promote the development of the brood patch. The brood patch is an area from which the female plucks the feathers so that she has direct skin contact with the eggs or hatchlings, improving her ability to warm the brood. In management of domestic poultry, such as chickens, females displaying nesting behavior and a brood patch due to high levels of prolactin are referred to as broody. If a farmer’s object is to have the female produce more eggs, behavioral interventions (preventing hens from spending time in their nest, for example) are used to attempt to prevent broodiness and thus keep the birds laying. Drugs that block dopamine may also prevent broodiness. In birds, prolactin also inhibits the ovaries from developing more eggs and promotes foraging behavior. Prolactin-induced weight gain may be an important preparation for migration.

In mammals, prolactin has many of the same effects. During pregnancy, prolactin levels increase, stimulating glandular development of the breasts. Prolactin primes maternal behavior and modulates stress that is associated with pregnancy and maternal care. Repeated pregnancies reinforce better maternal care, partly because each pregnancy induces more prolactin receptors in the brain; the larger number of receptors then enable stronger maternal responses. The inhibitory effect of prolactin on ovulation makes it unlikely that a nursing mammal will become pregnant; nursing can be an effective natural contraceptive. At least in humans, prolactin is also associated with sexual arousal and pleasure, due to its inhibition of dopamine secretion. The precise behavioral effects of prolactin and testosterone on parental behavior vary among species, but the general pattern is that prolactin enhances maternal behavior while testosterone inhibits or interferes with paternal behavior. Finally, oxytocin also causes muscular contractions in the uterus associated with birth and milk-letdown in milk production, and is thought to be important in maternal bonding with young animals.