Parenting Behavior

  

C H A P T E R

51 Parenting Behavior

  

Joseph S. Lonstein

Neuroscience Program and Department of Psychology, Michigan State University, East Lansing, MI, USA

  

Mariana Pereira, Joan I. Morrell

Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ, USA

  

Catherine A. Marler

Neuroscience Training Program and Department of Psychology, University of Wisconsin, Madison, WI, USA

  INTRODUCTION

  The reproductive venture in mammals typically begins with the task of choosing a mate and is followed by the copulatory interactions that culminate in the join- ing of ova and sperm. For almost all mammals, repro- duction and its behavioral correlates do not end there. Most mothers give birth to young that are unprepared for an independent life ex utero, thus requiring that the neonates receive prolonged and intense parental care for their sheer survival. Caregiving by most animals is highly sexually dimorphic,

  

  f- spring this nurturance is provided by their mothers and is termed maternal behavior. In animals that have a rela- tively rare reproductive strategy involving biparental care, fathers will provide paternal behavior. In addition, caregiving may not be restricted to the parents and can be displayed by other willing participants, including the neonate’s older siblings or other close relatives, who pro- vide beneficial alloparental behavior.

  Potential caregivers are often not spontaneously interested in young or may not be able to adequately care for them even if interested in doing so. Through the process of pregnancy and parturition, a profound neurobehavioral transition occurs in maternally inexpe- rienced female mammals such that any clumsiness or indifference to neonates, or even outright aggression toward them, is replaced by skillful and tender caregiv- ing. Of course, caregivers other than biological mothers do not gestate and give birth to offspring, so there must be alternative means that promote their nurturant behaviors.

  The literature detailing the physiology of mammalian parental behaviors has been reviewed numerous times with tremendous thought and detail. The goal of this

  chapter is not to again exhaustively review this large lit- erature, and we refer readers elsewhere for details not found herein.

  

  e instead highlight what we view as the major scientific advances in our understanding of the endocrinology, sensory regulation, and neurobiology of nurturant behaviors displayed by mothers, fathers, and sometimes alloparental “helpers.” Similar to the reductionistic study of most mammalian behaviors, the physiology of parenting is best understood in labora- tory rodents. This is justified by their exceptionally suc- cessful breeding within a laboratory environment, the broad social acceptance for their use in basic research, a wealth of existing knowledge about their endocrinol- ogy and neurobiology, and the important belief that such an evolutionarily conserved behavior as parenting will have similar biological underpinning across mammals. Indeed, sufficient investigation of nonrodent parents, including sheep, rabbits, and primates, provides rich- ness to this literature and ample data that allow one to detect potential universals, as well as species-specific mechanisms, involved in this biologically complex, incredibly motivated, and evolutionarily essential mam- malian social behavior.

51. PARENTING BEHAVIOR 2372

  Historical Perspective

  and the display of maternal-like behavior in male rats given anterior pituitary implants

  exogenous hormone treatment and no interest in pups begin to perform caregiving behaviors after repeated exposur

  

   about the endocrinology of mothering were not clari- fied, however, until as late as the 1960s. These included that neither PRL nor progesterone could alone promote maternal behavior in virgin female rats and instead required the assistance of other endocrine factors.

  

  One of these factors is now known to be estradiol, although at least two studies from the 1960s (which can era” for the biological study of maternal behavior) could not demonstrate estradiol’s effects, probably because the temporal sequences of the exogenous hormones given were endocrinologically incorrect (see the section

  

  

  Extant research on the hormonal regulation of caregiv- ing behaviors shown by male mammals also began almost a century ago, but often had the goal of inducing maternal- like behaviors in species of males that were not naturally paternal. These studies included observations of female- like interest in pups by guinea pigs and rats that were

  

  own

  Studying the biological mechanisms underlying parental behavior has a century-long history. Some of the earliest research on this topic refers to observational or experimental work on the endocrine, sensory, or neural basis of copulation in rodents and other small mammals; thus, we can presume that the study of parenting behav- ior arose from and was informed by the study of mat- ing behavior. Cross-fertilization between these fields still occurs today, which is understandable given the discrete set of sensory, endocrine, and neurobiological faculties that animals have available to conduct a wide range of reproductive and other social activities. Contemplating the similarities or differences among behaviors, such as parenting and mating, will continue to provide valuable insight into the biological mechanisms underlying them both.

  has more recently criticized this strategy as misguided for understanding paternal behavior in any naturally bipa- rental species because a female-oriented focus leads one to incorrectly assume that the endocrine and neural factors underlying maternal behavior are similarly responsible for

   As far as we can determine,

  the earliest work manipulating the endocrine system of any spontaneously paternal male mammal was studies from the 1930s that found no effects of hypophysectomy on the paternal behavior of male laboratory mice.

   Studies of

  the steroid hormones involved in a paternal male primate came much later, with Wilson and V

  

  report that castrated male rhesus macaques (Macaca mulatta)— albeit a species that is still not particularly paternal in natural environments—are particularly prone to exhibit paternal behaviors and Alexander’s 1970

  

   the androgen withdrawal occurring across seasons in the

  ous rats with no

  Early studies also demonstrated the still often-used paradigm of maternal “sensitization” (see

  

8 Such parabiotic studies were resurrected by Terkel and

  

  

  Questions asked in the very early studies of mother- ing were quite similar to those asked today. For exam- ple, the search for bloodborne factors that are released during pregnancy or lactation and involved in maternal

  

  surgically conjoined virgin and pregnant female rats in hopes of finding accelerated maternal responding in the conjoined virgin. Stone’s study was unsuccess- ful, but reasonable given that parabiotic methods had previously shown that bloodborne factors could travel from one animal to affect the physiology of another.

  Rosenblatt almost 50 years later, who did find enhanced maternal responding in the conjoined virgins (see the section

  

  The 1920s also saw reports that particular patterns of ovarian activity were correlated with mating in female rats and that ovarian hormones could induce copulation when exogenously administer

  

  Either in response to these studies, or simply consistent with the zeitgeist, a flurry of studies emerged soon thereafter reporting that mothering would be displayed by dogs given extracts from the urine of pr

  and that maternal behavior could be seen in a nulliparous monkey

  ) such that ovariectomy or hypophysectomy has little effect on postpartum mothers’ general inter-

  

   virgin rats

  ude extracts of the pituitary gland.

  The next few decades saw numerous, but often meth- odologically compromised and contradictory, studies attempting to pinpoint the ovarian and pituitary secre- tions that could induce or inhibit mothering. Some reported that ovarian hormones could only inhibit moth- ering,

  

   pituitary, or thyroid hormone could promote maternal behavior when given alone or in combination.

  amongst such discrepant results were findings that later became fundamental concepts in the current field study- ing parenting behavior. For example, prolactin (PRL) has been known for decades to promote the onset of mater- nal behavior in ovarian hormone–primed nulliparous rats.

  Also, it has long been known that after hormones

  promote the onset of maternal behavior in many species, endocrine factors are unnecessary for maintaining the behavior (through a process termed “eroticization” by

  

17 Buried

COMPONENTS OF PARENTAL CARE 2373

  more naturally paternal male Japanese macaque (Macaca

  

  now know about the roles of the preoptic area and ven- tromedial hypothalamus in maternal behavior (see the section these findings would be surprising if reported today. Other studies around this time found that lesions of the lateral hypothalamus, septum, hippocampus, or mammillary bodies disrupted mothering in female rats

  

  - late cortex could sometimes produce negative conse-

  

  It will be seen in this chapter that significant advances in experi- mental methodology—including more widespread use of and greater sophistication in neuroanatomical trac- ing, the ability to use genomic responses or regional oxygen utilization to visualize the activity of multiple brain sites simultaneously, and the development of techniques to manipulate the rodent genome—have permitted the field to move away from using lesions to conduct this type of site-by-site analysis of the neural structures required for parental behavior and instead provide a more network- or integrative systems-level behaviors (see the section

  By studying the effects of individual and multiple desensitizations on retrieval of pups, Beach and Jaynes laid the groundwork for our understanding that maternal responding in rats was under “multisensory control.” More recent studies re-examining the sensory control of retrieval and other the responses of human mothers to infant sensory cues, support many of Beach and Jayne’s early conclusions that no single sensory modality is indispensable for most

  later systematically provided many additional insights into this question, again partly drawing on previous work studying the sensory control of copulatory behavior in rats and other

  fuscata) was associated with males’ increased paternal

  

  With regard to the sensory control of parenting, there was evidence 80 years ago that blinding or anos- mia had little effect on nest building or other maternal

  dwarf hamsters (Phodopus campbelli)—began to emerge just less than two decades ago.

  cus californicus), prairie voles (Microtus ochrogaster), and

  ies of the now exemplar rodent models used to study the natural occurrence of fathering—California mice (Peromys-

   , endocrinological stud-

  play with young.

  

COMPONENTS OF PARENTAL CARE

  

  Starting in the 1930s, electrolytic or aspiration lesions were employed to study the central nervous system con- trol of maternal behavior, but these studies produced dis- crepant results for decades.

   ).

35 The cerebral cortex was the

  It is important to begin the discussion about the components of parental care by first highlighting that the nature of parental attraction to infants dif- fers considerably among species. Polytocous rodents such as laboratory rats, mice, and rabbits that give birth to many offspring can discriminate between their own and unrelated pups, but form no exclu- sive bonds with them. In laboratory environments, these mothers will indiscriminately care for any con- specific or even nonconspecific neonates. Such gen- erous mothering could be a laboratory artifact, but

  

  and aggressiveness toward potentially infanticidal intruders. This last modification is outside the scope of this review, so we refer readers elsewhere for informa- tion about the hormonal and neural control of maternal aggr

  

   cognitive skills that may optimize parental responding to the neonates and other aspects of the environment,

  

  Successful parenting results from parents’ increased attraction to infants, the perfection of infant-directed caregiving behaviors, and modification of existing capabilities that are not even oriented toward the off- spring but nonetheless promote their survival. Some of these modifications in non-offspring directed behav- iors include blunted emotional reactivity that may help par

  first focus of this work and, once again, it took some lead from research that had unsuccessfully sought to find the

36 In his studies

  eported that substantial decortication abolished maternal behav- ior. Later experiments did indicate cortical specificity for mothering,

  examining cortical control of mothering as an exemplar innate behavior, Beach found that the amount of cortical tissue loss was proportional to the temporospatial disor- ganization of the females’ maternal behaviors but that the location of the cortical loss was mostly irr

  

  Ar

  

   described how nest building and sometimes retrieval and licking the pups could be elicited in a small num- ber of male rats that received infusions of sodium testo- sterone sulfate into the medial, but not lateral, preoptic area. Prepartum lesions of the ventromedial preoptic area were later reported to have no consequence on postpartum maternal behavior, while ventromedial nucleus lesions elicited infanticide.

  

  The first clear evidence for a subcortical influence on caregiving behaviors came from Fisher in 1956,

  

   lesion effects on maternal behavior were partly due to

  and Davis

  

51. PARENTING BEHAVIOR 2374

  instead might be relevant in natural environments when lactating mothers communally nest.

  altricial rabbit pups receive only 3 min of maternal care each day.

  Cleaning the offspring is another

  and rabbits who nurse at the bottom of a deep burrow from which the pups cannot easily escape.

  

  birth, offspring-directed behaviors may seem to be a seamless thread of activities, but a closer look reveals that they are instead a collection of behavioral routines and subroutines that are appropriate to study both individu- ally and collectively. This study is often facilitated by care- ful observation of the individual behaviors displayed, and then grouping them into meaningful categories of activi- ties that might involve particular parts of the parents’ bodies, are most often temporally associated, or appear to have similar or interdependent purposes. This task can be difficult because not all mammalian parents display the same repertoire of behaviors and universal catego- rization of parental activities may be impossible. Even so, many researchers have distinguished active parental behaviors from inactive parental behaviors. Active paren- tal behaviors include many of the hallmarks of caregiving, including establishing a place where mother–offspring ing. For many animals, including most small rodents with altricial young, this involves transporting suitable materi- als to a central location and manipulating them into a safe and secure nest. Active parenting also often involves car- rying displaced offspring from one place to another using the mouth, hands, or arms, or more passively allowing the offspring to cling to the parent’s fur to hitch a ride. Car- rying or retrieving neonates is easily quantifiable in both the field and laboratory, but it is important to note that its propensity is not universal. It is mostly unnecessary and even impossible in precocious species with heavy or highly mobile young, and it is also rare even in some relatively altricial species. These include prairie voles (M. ochrogaster), whose pups are born with teeth that help maintain attachment to the mother

   Regardless of the neonate’s developmental stage at

  cies differences in the fat, protein, and water content of maternal milk allow such variation in the frequency of mammalian caregiving to exist.

   Spe-

  

57 In contrast to these altricial offspring, relatively

  

  In many mammals, these active maternal behav- iors are often performed in preparation for prolonged periods of inactive nursing, the behaviors involved in transferring mother’s milk to the infants. Lac- tation (i.e., milk production and letdown) is not a behavior, and there is a tremendous amount of infor- mation known about this physiological process that can be found elsewhere. (see Chapter 46; and ith regard to nursing behavior, in response to offspring suckling some mothers undergo a transi- tion from a highly active state to one of inactivity and quiescence, which in laboratory rats, cats, and primates

  Based on their developmental stage, one might expect that maternal care is frequent and protracted toward altricial young, but infrequent and brief toward preco- cious young. This is not necessarily the case. Startlingly, whereas altricial rat pups are in the nest with their moth- ers for 70–90% of the

  as sheep, horses, and guinea pigs; they are born furred, with eyes wide open, and are surprisingly mobile. Such differences between altricial and precocial young are relevant for understanding the relationships among the hormonal profiles of nonhuman animals, that of our own species, and females’ caregiving behaviors. One salient example is that while both the sheep (∼147 days) and human (∼280 days) have lengthy pregnancies, sheep give birth to precocious offspring, whereas human offspring are relatively altricial. The durations of hormone expo- sure in these species are more similar to each other than, say, to that of laboratory rats, but maternal interactions with young at parturition differ tremendously. Thus, the hormonal patterns during and after pregnancy, and the developmental state of the young at birth, must all be considered to accurately uncover the neurobiological mechanisms driving maternal care in any given species.

  offspring) often arise from longer gestating mammals such

  neurobehaviorally developed neonates (termed precocial

  tioned mammals, such as rodents, rabbits, dogs, and cats; at birth, they have a limited ability to thermoregulate, locomote, see, or hear. Even more extreme are the altri- cial young of some species that appear almost embryonic at birth, such as some marsupials that are born after an tal life within their mother’s pouch to seemingly finish up what was unaccomplished during in utero develop-

  altricial offspring) are often offspring of small, short-gesta-

  esponses tremendously depend on the characteristics of the offspring. These include the new- born’s neurobehavioral competency for independent sur- vival. Neurobehaviorally undeveloped neonates (termed

  

  There are also considerable differences among species in their parental repertoires, which often lies in the fact that parent–offspring interactions are necessarily dyadic, involving reciprocal stimulation between the partici- pants,

  - trast to these rodents, maternal sheep form an impres- sively selective bond with their offspring at parturition that prevents foster caregiving. Unlike either example, most human mothers form an intense bond with their infants, but this bond is not exclusive and the possibil- ity of caregiving toward other infants of course remains.

  common active parental behavior and is performed by nonprimates by using the mouth to lick or gently nibble, but in primates it also involves the parents’ hands.

59 Similarly, pre-

  e mem- bers of species that follow close behind their mothers and remain within steps of her most of the

  

  cocious ungulates are either “cached” away and visited by the mother just a few times per day

CONSIDERATIONS FOR UNDERSTANDING THE HORMONAL REGULATION OF MATERNAL CARE 2375

  

  

   of quiescence does milk letdown occur in rats.

70 In rab-

  bits and pigs, suckling elicits behavioral inactivity, but it is associated with increased cortical firing rather than a depression.

  

  -legged mothers that are simultaneously nursing multiple offspring will assume a distinctive posture, termed kyphosis,

  

   limb rigidity and an upward flexion of the spinal col- umn. This nursing posture provides additional room for young to breathe, move, and suckle while underneath their mother. Kyphosis is more likely to occur earlier in lactation than later and is the optimal position for milk

  In pregnant and postpartum mammals, the hormonal profiles of rodents and humans have been the best stud- ied, but some additional models including sheep have significantly added to our understanding of this topic. Each nonhuman animal model possesses different fea- tures of face, construct, and predictive validity for the hormonal basis of parenting in humans, but no single model provides a complete picture homologous to what is known from humans. Even so, each model holds uniquely useful characteristics for examining the emer- gence and continuation of maternal behavior. For exam- ple, a valuable feature of the laboratory rat model is that while rats do recognize their own young, their assidu- ous and rapid care for the young of other individuals facilitates many laboratory studies. On the other hand, a crucial and fascinating feature of caregiving in sheep is the selective mother–offspring bond, which is based on individual recognition and memory of lamb cues, and humans.

74 In

  The hormonal profile of pregnancy and the peripar- tum period is crucial for supporting the developing fetus, while at the same time prepares “the expectant brain” and the periphery for the expression of mater- nal behavior and other required physiological processes such as lactation (see Chapter 44). Extensive experi- mental evidence has demonstrated that estradiol, pro- gesterone, PRL, and sometimes oxytocin (OT) can play crucial roles in the onset of maternal behavior in rodents and ungulates, with the addition of cortisol important in primates. A remarkable feature of the hormonal pro- files over a wide range of species is the similarity of the hormones and their temporal course during preg- nancy, parturition, and the postpartum period. Another remarkable feature is that not only do the maternal ova- ries, adrenals, and anterior pituitary act as hormonal sources during pregnancy, as they do during all repro- ductive phases, but the placenta and fetus individually and together are also powerful sources of hormones unique to pregnancy that can act peripherally and per- haps centrally.

  Correlating hormone levels in the pregnant and par- turient female with the expression of maternal behaviors is an important approach to examining the hormonal basis for maternal behavior in all species examined, and really the only approach available to do so in humans. When considering the major changes in the hormonal milieu for the three exemplar species discussed in detail below, it is absolutely crucial to consider the extent to which the maternal brain is bathed in this milieu: that is, whether the blood–brain barrier does or does not prevent the hormones of interest from reaching the brain. It is generally accepted that steroid hormones readily access the brain, but most peptide hormones of peripheral origin are more highly regulated or almost completely restricted from access. Some peptides, including those in the PRL family, gain access via peptide-specific trans- porter systems that result in cerebrospinal fluid levels being highly correlated with plasma levels.

  ,

  less than 3% of most other peripherally circulating pep- tides without such transporter systems, including OT and arginine–vasopressin (A

   While

  there is limited evidence that the blood–brain barrier is not altered by pregnancy,

  

  the access of such peptides to the brain during this time has not been experimen- tally examined in detail, so great caution is warranted when attempting to extrapolate peripheral (plasma and saliva) peptide hormone titers to what may be found in the brain. In addition, the marked advantages of ani- mal models for examining the hormones necessary for the onset of maternal behavior allow experiments that provide causal evidence because the removal of glands

   CONSIDERATIONS FOR UNDERSTANDING THE HORMONAL REGULATION OF MATERNAL CARE

  addition to kyphosis, mothers can be readily observed lying prone on top of the young with little limb sup- port or found lying in a supine position next to or under the pups. These latter postures may be especially com- mon when mothers are either fatigued by the rigidity of kyphosis, when offspring are too large for the entire lit- ter to fit under her, or when older pups initiate nursing from a recumbent mother

  Basic information about this hormonal profile is essential for understanding the state changes in the female brain that increase maternal motivation and her readiness to provide care to the young. Because these hormones act on the periphery and brain via their respective families of hormone receptors, it is also criti- cally important to understand how reproductive state alters hormone receptor expression, affects the domi- nance of particular subcategories of receptors, and how these receptors are influenced by their ligands to influ- ence neuronal activity and maternal responding.

51. PARENTING BEHAVIOR 2376

  and supplementation of hormones are readily pos- sible. There are substantial limits to such reductionist approaches, however, because disrupting the endocrine and physiological demands of pregnancy, parturition, and lactation can inadvertently confound analysis of the behavioral outcomes of most interest.

80 A great deal of recent research on laboratory rats and

  impor-

  1968 and 1972 that injecting plasma from early-postpar- tum laboratory rats into virgins, or commingling their

   Rosenblatt and Terkel reported in

  Harking back to Stone’s early parabiotic studies examining if bloodborne factors were involved in moth- ering behaviors,

  Frequently encountered limits of the conditional activation systems include the complete- ness of the excision (i.e., a knockout that is really a knock- down), the confounding influence of the floxing itself, and the leakiness of Cre activation into off-target cells or tis- sues. In the best circumstances, proof of effectiveness and target specificity can mitigate these problems, while in the worst cases the KO model being studied does not allow one to make interpretable conclusions.

  

  tantly, the absence of some proteins during development may generate very different functional alterations than if the proteins are absent only during adulthood. While con- ditional gene inactivation approaches may limit some of these problems by allowing temporal or spatial restriction of the KO or knockin, they bring other issues that have recently been discussed in the context of the androgen r

  For studies of behavior after global or lifelong knock- outs of any protein, it is also necessary to consider the possibility that behavioral resilience or alteration might be due to redundant proteins that take a larger than usual role or compensation by functionally associated molecules tion is the case in which a ligand normally regulates the expression of its own receptor, for example regulation of the OT receptor by its ligand, but where the receptor is normal even in the absence of OT, suggesting that other molecules have taken over its usual r

  The brain itself is also a source of steroid hormones and peptides that act as neuromodulators, including OT and AVP. As would be expected for neuromodula- tors, site-specific release of OT and AVP has been con- firmed and can be independent fr

  Regardless of the form of genetic or other manipula- tion, experiments impacting natural postpartum mater- nal behavior offer the most interpretable data when quantitative information is included about parturition behavior to verify that offspring are delivered alive and cleaned of amniotic membranes, that offspring viability is measured soon after parturition (including litter size and weight in rodents), and that the mothers are lactat- ing normally (including repeated measurement of off- spring weight or postmortem mammary gland weights). Because of the dyadic nature of mothering, further cru- cial inclusions include regularly assessing offspring vigor and replacing any sickly young with healthy foster young of a similar age, and maintaining a species-typical number of offspring for each mother to interact with.

  making this a generalizable consideration important for all stud- ies examining the genetics of behavior.

  

  eful consideration of the variability in these baselines is crucial because high spontaneous maternal behavior may be confused with the impact of endo- crine system gene KO, which may be subtle in strains with spontaneous maternal caregiving. Thus, there is a heightened requirement in studies of transgenic mod- els to make a faithful comparison of the impact of the genetic manipulation on the baseline postpartum or vir- gin maternal performance in the same strain. This issue of “background matters” has also been demonstrated for male sexual behavior in gene-disr

  

  is invaluable to realize that transgenic manipulations of receptors of ligands that mediate the hormonal under- pinnings of maternal behavior can have the unintended consequence of altering fertility or the capacity to main- tain pregnancy and undergo parturition. This makes it impossible to examine the hormonal and other factors involved in naturally occurring postpartum behavior, but does permit investigation of how these females respond to pups after repeated exposure to them in a mater- nal sensitization paradigm (described in detail below), which is thought to be non–hormonally controlled. It is also important to recognize that the neurobiological con- trol of maternal-like responses in females that have not undergone pregnancy and parturition could differ from those that have experienced these reproductive events. Furthermore, because different strains of nulliparous rats and mice vary in their baseline maternal responsive- ness,

  mice has been devoted to studying how naturally occur- ring genetic variation among individuals or genetic manipulations reveal important features about the endocrine and other neurochemical bases of mothering. endocrine and neuroendocrine basis of maternal behav- ior have been carried out with transgenic laboratory mice, and most of these have used global and lifelong knockout (KO) of specific endocrine system genes.

  Although independent brain and peripheral release has been demonstrated, it is also the case that OT and AVP are released intracerebrally at parturition and dur- ing suckling in apparent coordination with peripheral release, suggesting a hormonally coordinated linking of central and peripheral events in mothers.

  

HORMONES MOST SIGNIFICANT FOR THE ONSET OF MATERNAL BEHAVIOR

HORMONES MOST SIGNIFICANT FOR THE ONSET OF MATERNAL BEHAVIOR IN RODENTS, SHEEP, AND HUMANS 2377

  circulatory systems, dramatically reduced the latency to show maternal responding (

  

  rans- ferring periparturitional blood was by far the most effective. An almost innumerable number of endocrine events occur across the weeks or months of pregnancy and parturition, and up to years of lactation depend- ing on the species. Are they all required for mothering behaviors? Responding to foster pups by laboratory rats increases dramatically in the final days of pregnancy, presumably in preparation for the litter’s appearance at parturition.

  

  that remain unresponsive to pups or even infan- ticidal through the end of pregnancy. In contrast to most laboratory rats, sheep do not become more maternal as parturition approaches and the visceral events of either natural delivery or experimen- tally produced vaginocervical stimulation are needed for motherhood and development of the mother–young bond. Indeed, epidural anesthesia is a major impedi- ment to the onset of their maternal behavior

  Even though the onset of mothering does not require the sensory input of parturition, including vaginocervi- cal stimulation, or the ingestion of placentae and amni- otic fluid, these factors can still have positive effects on mothering in some laboratory rats.

  

  aginocervical stimulation naturally received during parturition is required, however, for the onset of mothering in many female prairie voles (M. ochrogaster)

  

  

88 In laboratory rats, the duration of preg-

  Of course, success- ful pregnancies normally terminate with parturition, when offspring would naturally first be available to the female. Because some aspects of maternal behavior appear prepartum and are displayed by late-pregnancy terminated rats, the physical processes of parturition are

  

  and receipt of vaginocervical stimulation must occur within a short time frame before the appearance of a lamb to avoid its total rejection by the

   While treatment

  with exogenous estradiol, progesterone, and central OT can induce maternal responsiveness even without vagi- ficult to achieve than in the rat. In the natural situation, both peripheral and central systems are coordinated by the processes of parturition, and vice versa, for maternal behavior in ewes (discussed further below). In humans, the now common use of Caesarean delivery has revealed that vaginal delivery is not required for their maternal responsiveness, but vaginal delivery is associated with greater maternal neural and behavioral sensitivity to infant cues as well as more positive maternal mental

  

  haps related to the endocrine and other chemical factors released during parturition. While the hormonally induced changes to the mater- nal brain instituted by pregnancy and the peripar- tum period are vital for neural sensitivity to offspring cues and the display of maternal behavior in the early postpartum period, after parturition the presence of hormones becomes progressively less important. The maintenance of maternal behavior is instead regulated by interaction with the offspring, with the dyad becom- ing an interactive duo that produces changes in mater- nal behaviors according to the needs of the developing offspring. Indeed, mothers and offspring of probably all mammalian species spend progressively less time with each other as the offspring become more physi- cally and motorically independent.

  

  A nonhormonal maintenance of maternal behavior is supported by many studies showing that removal of the pituitary, ovary, or adrenal glands does not terminate postpartum maternal behavior.

   There may be some changes in postpartum

  maternal behavior after removal of these glands, but they are quite subtle compared to their role in the onset of maternal behavior. For example, adrenalectomy has

FIGURE 51.1 Mean and range of the number of days of pup expo-

  sure for nulliparous female rats to begin retrieving pups. Females were exposed to pups alone (Pup Induced), were exposed to pups after receiving an injection of blood plasma from a recently parturient and maternal female (M → V Injection), or were exposed to pups during and after a 6 h transfusion of blood from a recently parturient and maternal female (M → V Transfusion). Transfusion from a parturient female very rapidly induced retrieval in the nulliparous rats. Source: Modified from Terkel and Rosenblatt, 1972.

  nancy before surgically terminating it via Caesarean procedures is positively associated with females’ mater- nal responsiveness, and at least 16 days of rising estro- gens and exposure to placental hormones followed by the withdrawal of progesterone is needed for a robust onset of maternal behavior

  

51. PARENTING BEHAVIOR 2378

  e is no rela- tionship between sensitization during juvenile life and

  Source: Modified from Lonstein et al., 1999.

  ing the pups (bottom panel). Different letters above bars indicate sig- nificant differences between groups. Maternally sensitized nulliparous rats were deficient in both measures compared to postpartum mothers.

FIGURE 51.2 Duration of time (Mean + SEM) that suckled and nonsuckled postpartum rats, and maternally sensitized nulliparous rats, took to retrieve each pup to the nest (top panel) and spent lick-

  Hormones are clearly not required for human parent- ing. The most salient evidence for this is that the adoption of human children in times of need, or simply by pref- erence, yields fully parental adults obviously without

  

  The sensitization paradigm has been combined with knowledge about the hormonal progression of pregnancy to establish that after days 17–19 of pregnancy, female rats are fully maternal within one day of pup exposure. Addi- tionally, treating nulliparous female rats with exogenous hormones for 2 weeks using a profile roughly mimicking that of mid- to late pregnancy can quickly induce moth- ering. This can even be accomplished in male rats! The optimal sequence of hormones that can instill mothering in laboratory rats, and probably numerous other spe- cies, is now known to involve (1) first exposing animals to estradiol, (2) subsequent introduction of progesterone, (3) administering PRL near the conclusion of the ovarian steroid treatment, and (4) the withdrawal of progesterone at the very end of tr

  

  Sensitization has also been used in various strains of mice, but both laboratory house mice (Mus) and deer mice (Peromyscus) have high levels of baseline caregiv- ing, again an important but sometimes overlooked consideration regarding their use for studying the hor- monal or neural basis of maternal behavior. There is no evidence that nulliparous sheep are susceptible to any sensitization of maternal behavior, and sensitization has been demonstrated to not be readily achievable in other

  

  little effect on retrieval, nest building, and nursing in postpartum rats, but it does increase how long mothers lick their pups and alters where licking is focused on the pups’

  

  The relationship between sensitized and postpartum maternal behavior has also been compared within subjects, and there is a positive correlation between how rapidly adult nullip- arous rats sensitize and how often they later lick their own of

  

  The maternal-like behavior of sensitized rats may be impressive, but it does differ from the behavior of nat- urally parturient females in its deficient retrieval, pup ).

  

  In some species, mothering-like behavior is possible without undergoing pregnancy and parturition—which is sometimes common in parental males, juvenile sib- lings, or genetically related nulliparous adult females— indicating that there are multiple means by which the neural substrates for parenting can be activated. Most virgin adult and juvenile laboratory rats of both sexes can be experimentally stimulated to perform some them to pups. Because these caregivers cannot lactate, the health of the foster pups is maintained by once- or twice-daily rotation to lactating surrogates. The emer- gence of such pup-induced or sensitized maternal behavior in nulliparous female rats usually takes up to 6–10 days of exposure and alters females’ behavior from avoiding the pups to avid caregiving. This sensitized maternal caregiving is thought to be hormone indepen- dent because it is not prevented or even greatly delayed by removing the adult subject’s gonads, pituitary gland, or adrenals before initiating the exposur

   Mothering without Pregnancy or Parturition?

   postpartum interaction between the mother and infant optimizes ongoing mothering, although there seems to be continuing modulatory roles for maternal OT and cortisol in r

  

  Similarly in the ewe, after postparturi- tional acceptance of the lamb, hormones are not required for maintaining maternal care and the mother’s inter- action with the lamb is instead cr

  

HORMONES MOST SIGNIFICANT FOR THE ONSET OF MATERNAL BEHAVIOR IN RODENTS, SHEEP, AND HUMANS 2379

  pregnancy or parturition in the adoptive parent. As dis-

  

   human parental behavior is more heavily influenced by experiential and cultural factors that parents bring to caregiving. Cultural conditions can introduce factors that are unique and in some cases more difficult to the adoptive parent–child dyad (e.g., preadoptive abuse, abandonment, or long-term institutionalization), but adoption in humans is a remarkably robust and success- ful process for both parents and children under a wide

   range of circumstances.

  Endocrine Profiles of Pregnancy Involved in the Onset of Mothering Laboratory Rodents Estrogen: Circulating estrogens during pregnancy in

  rats and mice are generally low and similar to diestrus until about 16 days after insemination, after which there

  

  is a gradual incr when plasma levels of estradiol meet and exceed those found

  

  during the estr estrus (leading to sexual receptivity ∼9 h later), but cir- culating estrogens are otherwise low during early lac- tation, then slowly rise across midlactation and even more as weaning and the resumption of estrus cyclicity

  

  appr In early pregnancy, the corpora lutea resulting from the liberated ova produce the steroidogenic substrates for estrogen synthesis, as well as the estradiol itself, so only estrogens are pro-

  

  duced in large amounts. This differs from late preg- nancy, when the placentae produce the androgens that are released into the general circulation and from which

   estradiol is then produced by the corpora lutea.

  During lactation, the corpora lutea of pregnancy regress, and the corpora lutea of the postpartum ovulation

   become functionally dominant.

  The presence of estradiol always induces a more rapid onset of maternal behavior than that observed in

  

  ucial role in the preparatory nest building displayed prepartum and for the immediate onset of all other maternal behaviors at parturition. A rapid onset of maternal behavior can be induced by just the first 10–13 days of pregnancy, or in nulliparous rats by 10–13 days of treatment with exogenous estradiol, if the animals are then given a triggering dose of estra-

  

  diol. the females’ endo-

  Schematic representation of circulating plasma FIGURE 51.3

  crine state, even a single high dose of estradiol benzoate

  levels of estradiol (EST), progesterone (PROG), and prolactin

  can shorten the latency for nulliparous rats to show

  (PRL) across pregnancy and parturition in laboratory rats, labo-

  maternal behavior. In studies using a surgical model

  ratory mice, and sheep. Source: Modified from Rosenblatt and Siegel, involving hysterectomy of pregnant females with or 1981.

  without ovariectomy, there is a much more rapid onset of maternal behavior when the ovary and its secretion of

  

  estradiol r, this does not occur

51. PARENTING BEHAVIOR 2380

  

  

  egnancy, however, the rat placenta produces the androgenic substrate for synthe- sis of most estrogens. This results in a lesser known rise in circulating androgens (testosterone and dihydrotes- tosterone) from very low levels (0.4–0.8 ng/ml) early in pregnancy to sustained and remarkable levels (2.8 ng/ ml) during the second half of pregnancy

  

  These levels are very high compared to that seen in cycling females, in which testosterone and dihydrotestoster- one are found at 0.2 ng/ml to 0.4–0.5 ng/ml preceding the sur

  

  These levels in late-pregnant females are even higher than those seen in male rats (1.1–2.3

  

  - tion, androgen levels drop and remain low until estrus cycling recommences.

  Such elevated plasma testosterone has not been reported in pregnant sheep, but high testosterone titers have been observed in pr

  

  

   Testosterone: Testosterone is an obligatory precursor

  where again the locations of estradiol synthesis and its testosterone precursor are in different tissues. While no on maternal behavior in rats or mice, in rabbits it is per- haps uniquely involved in their nest building because it loosens chest hairs that females pull out and use to line

  

  Androgens act on androgen receptors (ARs) located in specific tissues of the reproductive system and sites within the brain. In the brain, ARs exist in abundance in both males and females, are found on both neurons and glia, and act genomically as well as possibly nongenomi- cally