Plasticity of the paternal brain: Effects of fatherhood on neural structure and function.

Care of infants is a hallmark of mammals. Whereas parental care by mothers is obligatory for offspring survival in virtually all mammals, fathers provide care for their offspring in only an estimated 5%-10% of genera. In these species, the transition into fatherhood is often accompanied by pronounced changes in males' behavioral responses to young, including a reduction in aggression toward infants and an increase in nurturant behavior. The onset of fatherhood can also be associated with sensory, affective, and cognitive changes. The neuroplasticity that mediates these changes is not well understood; however, fatherhood can alter the production and survival of new neurons; function and structure of existing neurons; morphology of brain structures; and neuroendocrine signaling systems. Although these changes are thought to promote infant care by fathers, very little evidence exists to support this hypothesis; in most cases, neither the mechanisms underlying neuroplasticity in fathers nor its functional significance is known. In this paper, we review the available data on the neuroplasticity that occurs during the transition into fatherhood. We highlight gaps in our knowledge and future directions that will provide key insights into how and why fatherhood alters the structure and functioning of the male brain.

Long-Term Effects of Fatherhood on Morphology, Energetics, and Exercise Performance in California Mice (Peromyscus californicus).

In male mammals that provide care for their offspring, fatherhood can lead to changes in behavioral, morphological, and physiological traits, some of which might constitute trade-offs. However, relatively little is known about these changes, especially across multiple reproductive bouts, which are expected to magnify differences between fathers and nonreproductive males. We evaluated consequences of fatherhood in the monogamous, biparental California mouse (Peromsycus californicus) across seven consecutive reproductive bouts. We compared breeding adult males (housed with sham-ovariectomized females) with two control groups: nonbreeding males (housed with ovariectomized females treated with estrogen and progesterone to induce estrous behavior) and virgin males (housed with untreated ovariectomized females). At five time points (before pairing, early postpartum of the first litter, late postpartum of the second litter, early postpartum of the sixth litter, and late postpartum of the seventh litter or comparable time points for nonbreeding and virgin males), we measured males' body composition, hematocrit, predatory aggression, resting metabolic rate, maximal oxygen consumption (V˙O2 max⁡), grip strength, and sprint speed. We also weighed organs at the final time point. We predicted that fathers would have lower relative body fat and lower performance abilities compared with control groups and that these effects would become more pronounced with increasing parity. Contrary to predictions, breeding and control males differed in surprisingly few measures, and the number and magnitude of differences did not increase with parity. Thus, our expectations regarding trade-offs were not met. As reported in studies of single reproductive events, these results suggest that fatherhood has few costs in this species when housed under standard laboratory conditions, even across multiple reproductive bouts.

Consequences of placentophagia by adult virgin male California mice (Peromyscus californicus).

Placentophagia increases parental motivation in sexually inexperienced adult female rodents. We hypothesized that placenta ingestion has similar effects in virgin male California mice (Peromyscus californicus), a monogamous rodent in which fathers provide extensive care for their offspring. To test this hypothesis, we administered either a conspecific's placenta in oil or oil alone to adult virgin males via oral gavage. One, 7 or 24 hours later, each male underwent a 1-hour behavior test with either an unfamiliar pup or a novel object marble), immediately after which the mouse was perfused and the brain collected. Neural activation (Fos-immunoreactivity) was quantified in brain regions involved in parental care (bed nucleus of the stria terminalis, medial preoptic area, amygdala). We found few significant effects of placenta treatment, but at 7 h post-gavage, placenta-treated males had decreased latencies to approach both pups and marbles, compared to oil-treated controls (p = 0.05). Placenta-treated males also showed lower Fos-immunoreactivity in the dorsal bed nucleus of the stria terminalis, irrespective of stimulus type, compared to controls, both 1 h (p = 0.04) and 7 h (p = 0.05) post-treatment. These results suggest that placentophagia does not directly affect paternal motivation but might increase willingness to interact with novel stimuli in virgin male California mice.

Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of male California mice.

Parental care by fathers enhances offspring survival and development in numerous species. In the biparental California mouse, Peromyscus californicus, behavioral plasticity is seen during the transition into fatherhood: adult virgin males often exhibit aggressive or indifferent responses to pups, whereas fathers engage in extensive paternal care. In this species and other biparental mammals, the onset of paternal behavior is associated with increased neural responsiveness to pups in specific brain regions, including the medial preoptic area of the hypothalamus (MPOA), a region strongly implicated in both maternal and paternal behavior. To assess possible changes in neural circuit properties underlying this increased excitability, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in adult male California mice that were either virgins or first-time fathers. We used standard whole-cell recordings in a novel in vitro slice preparation. Excitatory and inhibitory post-synaptic currents from MPOA neurons were recorded in response to local electrical stimulation, and input/output curves were constructed for each. Responses to trains of stimuli were also examined. We quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. Biocytin was injected into neurons during recording, and their morphology was analyzed. Most parameters did not differ significantly between virgins and fathers. However, we document a decrease in synaptic inhibition in fathers. These findings suggest that the onset of paternal behavior in California mouse fathers may be associated with limited electrophysiological plasticity within the MPOA.

Neural Regulation of Paternal Behavior in Mammals: Sensory, Neuroendocrine, and Experiential Influences on the Paternal Brain.

Across the animal kingdom, parents in many species devote extraordinary effort toward caring for offspring, often risking their lives and exhausting limited resources. Understanding how the brain orchestrates parental care, biasing effort over the many competing demands, is an important topic in social neuroscience. In mammals, maternal care is necessary for offspring survival and is largely mediated by changes in hormones and neuropeptides that fluctuate massively during pregnancy, parturition, and lactation (e.g., progesterone, estradiol, oxytocin, and prolactin). In the relatively small number of mammalian species in which parental care by fathers enhances offspring survival and development, males also undergo endocrine changes concurrent with birth of their offspring, but on a smaller scale than females. Thus, fathers additionally rely on sensory signals from their mates, environment, and/or offspring to orchestrate paternal behavior. Males can engage in a variety of infant-directed behaviors that range from infanticide to avoidance to care; in many species, males can display all three behaviors in their lifetime. The neural plasticity that underlies such stark changes in behavior is not well understood. In this chapter we summarize current data on the neural circuitry that has been proposed to underlie paternal care in mammals, as well as sensory, neuroendocrine, and experiential influences on paternal behavior and on the underlying circuitry. We highlight some of the gaps in our current knowledge of this system and propose future directions that will enable the development of a more comprehensive understanding of the proximate control of parenting by fathers.

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation.

Parental care by fathers, although rare among mmmals, can be essential for the survival and normal development of offspring in biparental species. A growing body of research on biparental rodents has identified several developmental and experiential influences on paternal responsiveness. Some of these factors, such as pubertal maturation, interactions with pups, and cues from a pregnant mate, contribute to pronounced changes in paternal responsiveness across the course of the lifetime in individual males. Others, particularly intrauterine position during gestation and parental care received during postnatal development, can have long-term effects on paternal behavior and contribute to stable differences among individuals within a species. Focusing on five well-studied, biparental rodent species, we review the developmental and experiential factors that have been shown to influence paternal responsiveness, and consider their roles in generating both intra- and inter-individual variation. We also review hormones and neuropeptides that have been shown to modulate paternal care and discuss their potential contributions to behavioral differences within and between males. Finally, we discuss the possibility that vasopressinergic and possibly oxytocinergic signaling within the brain, modulated by gonadal steroid hormones, may represent the "final common pathway" mediating effects of developmental and experiential variables on intra- and inter-individual variation in paternal care.

Effects of repeated pup exposure on behavioral, neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus).

In biparental mammals, the factors facilitating the onset of male parental behavior are not well understood. While hormonal changes in fathers may play a role, prior experience with pups has also been implicated. We evaluated effects of prior exposure to pups on paternal responsiveness in the biparental California mouse (Peromyscus californicus). We analyzed behavioral, neural, and corticosterone responses to pups in adult virgin males that were interacting with a pup for the first time, adult virgin males that had been exposed to pups 3 times for 20min each in the previous week, and new fathers. Control groups of virgins were similarly tested with a novel object (marble). Previous exposure to pups decreased virgins' latency to approach pups and initiate paternal care, and increased time spent in paternal care. Responses to pups did not differ between virgins with repeated exposure to pups and new fathers. In contrast, repeated exposure to a marble had no effects. Neither basal corticosterone levels nor corticosterone levels following acute pup or marble exposure differed among groups. Finally, Fos expression in the medial preoptic area, ventral and dorsal bed nucleus of the stria terminalis was higher following exposure to a pup than to a marble. Fos expression was not, however, affected by previous exposure to these stimuli. These results suggest that previous experience with pups can facilitate the onset of parental behavior in male California mice, similar to findings in female rodents, and that this effect is not associated with a general reduction in neophobia.