Prolactin action is necessary for parental behavior in male mice

Parental care is critical for successful reproduction in mammals. In comparison to maternal care, the neuroendocrine mechanisms supporting paternal care are less well-studied. Laboratory mice show a mating-induced suppression of infanticide (normally observed in virgins) and onset of paternal behavior. Using this model, we sought to investigate whether the hormone prolactin plays a role in paternal behavior, as it does for maternal behavior. First, using c-fos immunoreactivity in Prlr-IRES-Cre-tdtomato reporter mouse sires, we show that the circuitry activated during paternal interactions contains prolactin-responsive neurons, including the medial preoptic area, bed nucleus of the stria terminalis, and medial amygdala. To evaluate whether prolactin action is required for the establishment and display of paternal behavior, we conditionally deleted the prolactin receptor (Prlr) from 3 distinct cell types: glutamatergic, GABAergic, and CaMKIIα-expressing forebrain neurons. Prlr-deletion from CaMKIIα-expressing forebrain neurons, but not from glutamatergic or GABAergic cells, resulted in a profound effect on paternal behavior, as none of these males completed the pup retrieval task. Finally, although sires do not show an acute increase in circulating prolactin levels in response to pups, pharmacological blockade of prolactin-release at the time of pup exposure resulted in failure to retrieve pups, similar to when the Prlr was deleted from CaMKIIα neurons, with prolactin administration rescuing this behavior. Taken together, our data show that paternal behavior in sires is dependent on basal levels of circulating prolactin acting at the Prlr on CaMKIIα-expressing neurons. These new data in male mice demonstrate that prolactin has a similar action in both sexes to promote parental care.

Behavioral Endocrinology: Integrating Mind and Body

The nervous system and the endocrine system interact to integrate behavior and physiology. Hormones play an important role in this interaction, particularly steroid hormones. Other molecules, notably oxytocin, can serve both as hormones in the soma and neuromodulators in the central nervous system. Understanding the influence of the endocrine system on human behavior, both individual and social, has been a primary focus of behavioral endocrinology for many decades, though technical and methodological challenges have been formidable. The recent enthusiasm for enzyme-linked immunoassay kits for measuring steroid hormones in saliva has been found to be largely unsound, for example. Despite these difficulties, advances in many areas have been made and new areas, such as the endocrinology of paternal behavior and the role of oxytocin in social interactions, have emerged. Reproductive ecology provides a theoretical framework for integrating the diverse content of human behavioral ecology.

Alloparental Behavior and Paternal Behavior in Nonhuman Mammals

Chapter 7 examines alloparental and paternal behavior. Although these behaviors are rare in mammals, their occurrence indicates that parental behavior can occur in the absence of pregnancy and parturition. For mammals of both sexes, dual brain circuits affect whether parental behavior occurs: An inhibitory defensive circuit (anterior hypothalamus/ventromedial hypothalamus projections to periaqueductal gray), and an excitatory parental circuit (medial preoptic area, mesolimbic dopamine system, and the oxytocin system). When alloparental behavior occurs, either through experimental genetic selection (virgin female laboratory house mice) or through natural selection (prairie voles, marmosets), the defensive circuit has been downregulated and the parental circuit has been upregulated by such selection. When paternal behavior occurs, either naturally (California mice, dwarf hamsters) or experimentally (laboratory rats and house mice), copulation with a female and remaining with her through parturition depresses the male’s defensive circuitry while activating his parental circuitry.

Parental Behavior

Chapter 2 describes the types of parental behavior that can occur in vertebrates: maternal, paternal, and alloparental behavior. The dominant form of parental behavior in mammals is a uniparental maternal care system, where the mother raises her offspring by herself. A mother can form either a nonselective or selective bond with her infants, depending on the maturity of her infants at birth. A biparental care system, in which both maternal and paternal behavior occur, is present in about 5% of mammalian species. Approximately 3% of mammalian species exhibit a cooperative breeding system, where some offspring remain in their social group and help their parents raise subsequent offspring. The parental behavior of these helpers is referred to as alloparental behavior. The occurrence of paternal and alloparental behavior shows that alternative mechanisms, not requiring pregnancy and parturition, can evolve which allow for these forms of parental behavior.

The Parental Brain

The Parental Brain: Mechanisms, Development, and Evolution takes a three-pronged approach to the parental brain. The first part of the book deals with neural mechanisms. Subcortical circuits are crucially involved in parental behavior, and, for most mammals, the physiological events of pregnancy and parturition prime these circuits so that they become responsive to infant stimuli, allowing for the onset of maternal behavior at parturition. However, since paternal behavior and alloparental behavior occur in some mammalian species, alternate mechanisms are shown to exist that regulate the access of infant stimuli to these circuits. In humans, cortical circuits interact with subcortical circuits so that parental feeling states (emotions) and cognitions can be translated into parental behavior. The section on development emphasizes the experiential basis of the intergenerational continuity of normal and abnormal maternal behavior in animals and humans: The way a mother treats her infant affects the development of the infant’s brain and subsequent maternal behavior. Genetic factors, including epigenetic processes and gene by environment (G × E) interactions, are also involved. The chapter on evolution presents evidence that the parental brain most likely provided the foundation or template for other strong prosocial bonds. In particular, cortical and subcortical parental brain circuits have probably been utilized by natural selection to promote the evolution of the hyper-cooperation and hyper-prosociality that exist in human social groups. A unique aspect of this book is its integration of animal and human research to create a complete understanding of the parental brain.

The Psychometric Properties of the Persian Version of Childhood Experience of Care and Abuse Questionnaire (CECA)

Background: The present study aimed to determine the psychometric properties of the Persian version of the Childhood Experience of Care and Abuse Questionnaire (CECA.Q), a tool based on a retrospective interview with the child. Materials and Methods: To this aim, 251 adolescents from four regions of Tehran megacity completed the questionnaire. The reliability of the questionnaire was examined, along with the face and content validity. In addition, the construct validity was evaluated by exploratory factor analysis (EFA) and confirmatory factor analysis (CFA). Results: EFA and CFA supported a 4-factor solution including mother’s role scale items, father’s role scale items, maternal behavior scale items, and paternal behavior scale items. The total variance extracted in EFA ranged from 33.9 to 60.7. The internal consistency for mother’s role, father’s role, maternal behavior, and paternal behavior was 0.61, 0.65, 0.86, and 0.9 respectively. Thus, the questionnaire had a suitable fit, as well as reasonable reliability and validity. Conclusion: The Persian version of the CECA.Q had adequate reliability and validity as a self-report measurement for childhood experience of care and abuse. [GMJ.2020;9:e1663]

Paternal Behavior from a Neuroendocrine Perspective

How hormones and neuromodulators initiate and maintain paternal care is important for understanding the evolution of paternal care and the plasticity of the social brain. The focus here is on mammalian paternal behavior in rodents, non-human primates and humans. Only 5% of mammalian species express paternal care, and many of those species likely evolved the behavior convergently. This means that there is a high degree of variability in how hormones and neuromodulators shape paternal care across species. Important factors to consider include social experience (alloparental care, mating, pair bonding, raising a previous litter), types of care expressed (offspring protection, providing and sharing food, socio-cognitive development), and timing of hormonal changes (after mating, during gestation, after contact with offspring). The presence or absence of infanticide towards offspring prior to mating may also be a contributor, especially in rodents. Taking these important factors into account, we have found some general trends across species. (1) Testosterone and progesterone tend to be negatively correlated with paternal care but promote offspring defense in some species. The most evidence for a positive association between paternal care and testosterone have appeared in rodents. (2) Prolactin, oxytocin, corticosterone, and cortisol tend to be positively correlated. (3) Estradiol and vasopressin are likely nuclei specific—with some areas having a positive correlation with paternal care and others having a negative association. Some mechanisms appear to be coopted from females and others appear to have evolved independently. Overall, the neuroendocrine system seems especially important for mediating environmental influences on paternal behavior.