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.

Development of the Parental Brain in Humans

Chapter 10 deals with the development of the parental brain in humans, emphasizing experiential influences on the intergenerational continuity of maternal behavior: A history of experiencing childhood maltreatment (CMT; maternal neglect and/or abuse) is associated with alterations in the development of the child’s parental brain, which may lead to subsequent deficits in its maternal behavior. The manner in which parents treat their children may affect the development of neural systems (a) that regulate emotionality, with poor parental care resulting in deficits in emotion regulation, and (b) that underpin maternal motivation, love, and empathy, with poor parental care decreasing these processes. Alterations in the development of medial prefrontal cortex, amygdala, mesolimbic dopamine, oxytocin, corticotropin-releasing factor, and serotonin neural systems are involved, as are epigenetic effects. Not all mothers who experience CMT become poor mothers, and the involvement of gene by environment interactions are highlighted.

Anxiety Reduction and Maternal Aggression in Postpartum Nonhuman Mammals

Chapter 6 explores the neural mechanisms that regulate the decrease in anxiety and increase in maternal aggression that co-occur in postpartum mammals. Too much anxiety antagonizes maternal aggression. Therefore, postpartum anxiety reduction promotes maternal aggression. The neural circuitry of maternal aggression includes projections from the ventromedial nucleus of the hypothalamus to the periaqueductal gray and to other brainstem sites. Anxiety-related behaviors are mediated by corticotropin-releasing factor (CRF) neurons, and the projection of central nucleus of amygdala (CeA) CRF neurons to the dorsal bed nucleus of the stria terminalis is involved. Neural circuits are described to show how enhanced CRF release can depress maternal aggression. These circuits are typically downregulated in postpartum females, and oxytocin (OT) is involved. OT exerts anxiolytic effects and one mechanism of OT action is to depress the output of CeA.

Brain Mechanisms Regulating Maternal Behavior in Nonhuman Mammals

Chapter 4 examines the roles of oxytocin (OT) and olfaction in the maternal behavior of nonhuman mammals. It also presents an overview of brain anatomy. In concert with pregnancy hormones, the release of OT into the brain, derived from the paraventricular hypothalamic nucleus, stimulates the onset of maternal behavior. Although OT is not required for the maintenance of maternal behavior, it does enhance maternal behavior during the postpartum period in challenging environments by decreasing anxiety and increasing maternal motivation. OT, in the absence of pregnancy hormones, may also enhance maternal responsiveness in alloparents. For many postpartum mammals, maternal motivation is under multisensory control, and olfaction is not required, although it is necessary for maternal selectivity in sheep. In contrast, for laboratory mice, olfaction is essential for maternal motivation. For virgin female rats and rabbits, olfactory input from pups inhibits maternal behavior, but this inhibition is eliminated at parturition.

Central Neural Circuits Regulating Maternal Behavior in Nonhuman Mammals

Chapter 5 reviews the brain circuits that regulate maternal behavior in nonhuman mammals. The medial preoptic area (MPOA) is essential for both the onset and maintenance of maternal behavior. Hormones and oxytocin act on the MPOA to stimulate the onset of maternal behavior. The neurotransmitters contained within MPOA neurons that may regulate maternal behavior are described, as are several neural inputs to the MPOA that regulate its output. A defensive neural circuit that inhibits maternal behavior in most virgin female mammals is described. MPOA output stimulates maternal behavior by depressing the defensive circuit while also activating neural circuits that underpin maternal motivation. MPOA output to the mesolimbic dopamine system is essential for appetitive maternal responses, while its output to the periaqueductal gray regulates consummatory responses. Synaptic plasticity within the MPOA-to-mesolimbic DA circuit is involved in the development of an enduring mother–infant bond.

Introduction

The introduction provides a brief overview of the book, describing its three major themes: (a) the mechanisms through which the brain regulates parental behavior in nonhuman mammals and parental cognitions, emotions, and behavior in humans; (b) the experiential and genetic factors that affect the development of the parental brain, with a focus on the intergenerational continuity of normal and abnormal parental behavior; and (c) an evolutionary perspective based on the fact that maternal behavior is the most basic mammalian caregiving system. It is proposed that the parental brain served as a foundation upon which natural selection acted to result in the evolution of other forms of strong prosocial behaviors in mammals, including humans.

Evolutionary Perspectives on the Parental Brain

Chapter 11 presents evolutionary perspectives on the parental brain. First, the evolution of neural modifications to the parental brain that may have allowed for the emergence of alloparental behavior is re-examined. Second, evidence is presented for the proposal that the parental brain provided the foundation or template for the evolution of other types of strong prosocial bonds in mammals, such as the pair bond that occurs in biparental monogamous species, and the hyper-cooperation and hyper-prosociality directed toward in-group members, as opposed to out-group members, that occur in human societies. With respect to the latter, neural mechanisms associated with alloparenting and cooperative breeding may have served as a preadaptation. Neural models, along with evidence, are presented to show how cortical and subcortical parental brain circuits may have been appropriated and utilized by natural selection to result in the evolution of high levels of prosociality within human social groups.

Development of the Parental Brain in Nonhuman Mammals

Chapter 9 examines the development of the parental brain in animals, emphasizing that the way a mother treats her offspring affects their brain development and their subsequent maternal behavior, leading to an intergenerational continuity of maternal phenotypes. Two proposals are evaluated. First, maternal treatment influences the development of maternal motivation circuits in offspring. In support, the development of medial preoptic area projections to the mesolimbic dopamine system is affected. Second, maternal treatment influences the development of neural systems that regulate anxiety and stress reactivity in offspring. In support, the development of medial prefrontal cortex regulation of amygdala reactivity to stressful situations is affected. Deficient development of maternal motivation circuits may contribute to neglectful maternal behavior; deficient development of emotion regulation circuits may contribute to abusive maternal behavior. Epigenetics, particularly DNA methylation, and gene by environment interactions are involved in these processes.

The Parental Brain in Humans

Chapter 8 reviews the human parental brain. Most functional magnetic resonance imaging research has examined the maternal brain, with some research on the paternal brain. Although woman show allomaternal behavior, defensive neural circuits may depress maternal responsiveness under certain conditions. The subcortical circuits associated with human maternal behavior match those in nonhuman mammals and include medial preoptic area, mesolimbic dopamine, amygdala, and oxytocin neural systems. Interacting with these subcortical circuits are cortical regions, including dorsomedial prefrontal cortex and anterior insula, that are involved in maternal cognitions, empathy, emotions, and emotion regulation. The medial prefrontal cortex connects some of these cortical regions with the subcortical circuitry so that maternal cognitions and emotions can be translated into appropriate maternal behavior. The poor maternal behavior associated with postpartum depression may result from dysfunctions within these circuits, and alterations in corticotropin-releasing factor and OT may be involved.