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Regulatory role of prolactin in paternal behavior in male parents: A narrative review F Hashemian, F Shafigh, E RoohiDepartment of Clinical Pharmacy, Faculty of Pharmacy, Islamic Azad University, Pharmaceutical Sciences Branch, Tehran, Iran
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0022-3859.186389
In all mammalian species, a combination of neuroendocrine and experiential factors contributes to the emergence of remarkable behavioral changes observed in parental behavior. Yet, our understanding of neuroendocrine bases of paternal behavior in humans is still preliminary and more research is needed in this area. In the present review, the authors summarized hormonal bases of paternal behavior in both human and nonhuman mammalian species and focused on studies on the regulatory role of prolactin in occurrence of paternal behavior. All peer-reviewed journal articles published before 2015 for each area discussed (parental brain, hormonal bases of maternal behavior, hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in nonhuman mammalian species, hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in humans) were searched by PubMed, Medline, and Scopus for original research and review articles. Publications between 1973 and 2015 were included. Similar to female parents, elevated prolactin levels in new fathers most probably contribute to child-caring behavior and facilitate behavioral and emotional states attributed to child care. Moreover, elevated parental prolactin levels after childbirth decrease the parents' libidos so that they invest more in parental care than in fertility behavior. According to the available clinical studies, elevation in the amounts of prolactin levels after childbirth in male parents are probably associated with paternal behavior observed in humans. Keywords: Parental behavior, paternal behavior, prolactin
Currently, available data seem to be consistent with a working hypothesis that the expression of parental behavior involves neuroendocrine circuits in both male and female parents. Indeed, several studies indicated that the role of hormones such as estrogen, testosterone, oxytocin, vasopressin, and prolactin might be of great significance in organizing the neuronal machinery during early development, which sets the parameters for the amount of parental behavior observed. [1] Yet, little research has been done on the hormonal bases of paternal behavior and changes in reproductive endocrinology after childbirth in humans. Thus, understanding the neuroendocrinology of paternal behavior is an emerging research opportunity in behavioral neuroscience, [2],[3] which potentially could pave the way for translation of basic science findings into clinical settings. Schradin and Anzenberger emphasized the role of prolactin in the occurrence of paternal behavior and suggested that prolactin deserves the label of "hormone of paternity." Yet, given the fact that prolactin plays a significant role in the occurrence of both paternal and maternal behaviors, they concluded that it might indeed more properly be called the "hormone of parenthood." [4] To date, few clinical studies examined the hormonal influences of paternal care after childbirth. The present review aimed to summarize the available data on hormonal influences of paternal behavior in human and nonhuman mammalian species. Search Methods All peer-reviewed journal articles published before 2015 for each area discussed (parental brain, hormonal bases of maternal behavior, hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in nonhuman mammalian species, hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in humans) were searched by PubMed, Medline, and Scopus for original research and review articles. Publications between 1973 and 2015 were included. Parental brain For all female mammalian species, the reproductive experience alters the neurobiological processes in order to facilitate behavioral changes associated with parenting. Considerable research has been devoted to the understanding of the neuroendocrine pathways underlying maternal care in rodents and primates. [5] However, in only 6% of the mammalian species, including humans, intense paternal care has been manifested. [6],[7],[8] According to Leuner et al., less is known about neuroendocrine mechanisms underlying paternal behavior; however, the available evidence suggests that similar neuromodulators and hormones are responsible for parenting behavior in both men and women. [5] Similar brain regions, including prefrontal cortex, olfactory bulb, medial preoptic area, lateral septum, bed nucleus of the stria terminalis, and amygdala have been identified to be involved in the display of parental behavior. [9],[10],[11] Thus, parental brains clearly differ from those of nonparents, having been changed by the presence of the newborn and corresponding hormonal changes. [5] Hormonal bases of maternal behavior The influence of pregnancy and parturition hormones on maternal behavior has long been the topic of interest and research. [12] Extensive studies on rats and other mammals have demonstrated that high hormonal levels of oxytocin, prolactin, and estradiol by the end of pregnancy provide the basis for maternal behavioral changes. [13],[14],[15],[16],[17],[18],[19] A similar hormonal pattern (although the actual estrogen and progesterone profile in humans differ somewhat from that of other mammals) is found to be present in human mothers, which is responsible for parental behavior and feelings of attachment toward the newborn. [20],[21],[22] In fact, maternal behavior serves as the primary symbol for the human capacity to love and probably identifies the highest form of human intimacy. [23] Furthermore, researchers suggest that hormonal changes after childbirth lead to decreased libido of the parents and thus, contribute to increased parental investments. [1],[3],[24],[25] In fact, decreased libidos result from elevated prolactin and decreased testosterone levels in both male and female parents. [24],[25],[26] In this way, new parents are more likely to contribute to infant care and maximize the child's benefits and survival. To look at the issue from another perspective, one may argue that the importance of a good sexual function for individuals is indeed undeniable. [27] Although androgen levels are normally lower in females than males, researchers suggest that there is a positive correlation between decreased androgen levels and female sexual dysfunction. [28],[29] Turna et al. found significant differences in the total testosterone, free testosterone, and dehydroepiandrosterone blood levels of women with low libidos and the healthy controls. However, they argued that little is known about abnormal androgen level values in both pre- and postmenopausal women and whether those values directly correlate with sexual function. [28] In a novel study, Hashemian et al. found no direct correlation between sexual function and serum levels of androstanediol glucuronide in otherwise healthy married women. Thus, they concluded that the libido of a married woman probably cannot be predicted based on blood levels of androstanediol glucuronide. Moreover, they found no relationship between serum levels of T3, T4, thyroid-stimulating hormone (TSH), total testosterone, free testosterone, dehydroepiandrosterone sulfate (DHEA-S), and sexual dysfunction in otherwise healthy married women. [30] Yet, the role of decreased androgen levels and lowered libido cannot be denied. However, in the context of child-rearing, the mentioned physiologic decline in testosterone levels in both male and female parents contributes to infant care and maximizes the level of attention and affection parents give to the newborn. Hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in nonhuman mammalian species Mammalian paternal care is less common than maternal care due to differences in selective pressure during evolution. Given the specialized female reproductive physiology, female mammals can rarely increase their reproductive success by initiating a new pregnancy; however, males can increase their reproductive success by caring for offspring or by mating with other females. Paternal behavior in mammals has evolved separately in a number of linages where both parents are involved in parenting behavior due to environmental conditions. [1] Fewer studies have been conducted on the role of prolactin in mammalian male reproductive behavior, especially in relation to its probable effect on regulating paternal behavior after childbirth. [31] Paternal care increases survival of the offspring in Norway rats (Rattus norvegicus), [7] dwarf hamsters (Phodpus cambelli), [32] cotton-top tamarins (Saguinus oedipus), [33] marmosets (Callithrix jacchus), [34] and meerkats (Suricata suricatta). [35] According to Lonstein and De Vries, mice (Mus musculus) can show great variability in parental behavior across different studies. This is probably due to several factors including genetic and domestication influences. [7] The hormonal basis of parental behavior in male California mice (Peromyscus californicus) is not fully understood; however, plasma prolactin levels are found to be higher in fathers than in other males. [36] Norway rats (Rattus norvegicus) are probably the most extensively studied species with regard to maternal and paternal responsiveness. [7] Numerous studies demonstrated the influence of postnatal gonadal hormones on paternal responsiveness in adult male rats. The most common finding was that gonadectomy before puberty decreases infanticide and increases parental behavior. [37],[38],[39] Moreover, prolactin was found to affect parental responsiveness in adult rats [40] and was found in a greater ratio in juvenile males than juvenile females. [41] The Djungarian hamsters (Phodopus sungorus) exhibit biparental behavior as well. The exact underlying hormonal mechanism is unknown; however, an increase in testosterone after mating and its precipitous decline after birth of the offspring concomitant with an increase in plasma prolactin levels has been suggested to play a significant role in regulating parental behavior. [42] However, a study on the Djungarian hamster (Phodopus sungorus) indicated that administration of dopamine agonists, which suppresses prolactin production, failed to alter paternal behavior. [43] This may be due to the fact that numerous mechanisms are involved in the regulation of prolactin levels. Although the inhibitory effects of hypothalamic dopaminergic neurons in prolactin secretion have been well-established, other factors within the brain and peripheral organs have been known to stimulate prolactin secretion as well. [44] For instance, thyrotropin-releasing hormone, vasoactive intestinal polypeptide, vasopressin, serotonin, angiotensin II, prolactin-releasing peptide, and oxytocin are among the candidates suggested for being prolactin-releasing factors. [45] Ziegler and Snowdon found elevated prolactin levels in male cotton-top tamarins (Saguinus oedipus) during the mate's third gestational month. Moreover, an experienced male showed elevated prolactin levels and some inexperienced males demonstrated elevated prolactin just before parturition, suggesting noninfant cues were important as well. [33] Dixson and George also found significant higher prolactin levels in male cotton-top tamarins (Saguinus oedipus) who were fathers compared to nonfathers. [46] However, Almond et al. who suppressed prolactin production in paternally experienced common marmosets (Callithrix jacchus) found that experienced male marmosets could probably express paternal behavior in the absence of high prolactin levels normally seen after the birth of the offspring. [47] This may be due to the fact that parental behavior is affected by other variables such as experiential, cognitive, and social variables as well as biological variables, [48] and the parental behavior of nonhuman primates, particularly of those phylogenetically closest to humans (i.e., monkeys and apes as well as common marmosets) is more sensitive to experiential, cognitive, and social variables than the parental behavior of the other mammals. [49] Hormonal bases of paternal behavior and the role of prolactin in regulation of paternal behavior in humans Prolactin is probably best known for its role in lactation and maternal nurturing behavior; however, it is influential over approximately 300 biological functions across species [44],[50] leading it to be identified as the most versatile of all hormones. [24] Moreover, Ben-Jonathan et al. suggested that prolactin serves a dual function - both as a circulatory hormone and as a cytokine. [51] Prolactin is a polypeptide hormone that is synthesized and secreted from lactotrophs of the anterior pituitary gland, decidua, myometrium, breast, lymphocytes, leukocytes, and prostate. [44],[51] Evidence from cross-species studies suggests that prolactin has independently evolved to promote paternal investment in three distinct lineages: fish, birds, and mammals. [4] It may be very likely that prolactin has evolved to serve a similar function in the hominin lineage to the modern Homo sapiens.[52],[53] Similar to other species, human fathers and mothers show gender-specific parental behavior. [23] For instance, fathers seem to engage in more playful interactions that induce high positive arousals [54] while mothers prefer to establish face-to-face and affectionate interactions. [55] Thus, maternal and paternal behaviors most probably prepare children for different elements of future social behavior. Indeed, maternal care establishes a sense of safety within children while paternal behavior prepares them for elements of novelty and excitement, which are essential components of lasting social relationships. [23] Little research has been done on hormonal and behavioral changes that expectant fathers undergo prior to and after the birth of their children. [2],[25] One of the most comprehensive studies conducted on hormonal changes in male parents after childbirth was by Storey et al. The researchers studied the hormonal levels of testosterone, estrogen, prolactin, and cortisol in 33 parents at intervals prior to and after the birth of their children. They observed elevation and decline in the levels of the mentioned hormones in men during their partner's pregnancy. They found a 33% drop in testosterone levels in male parents during the first 3 weeks in the postpartum period. However, testosterone levels returned to normal by the time the infant was 4-7-week-old. The researchers suggested that the mentioned decline in males' testosterone levels after becoming a parent probably promoted attachment and regulated paternal behavior. Additionally, estrogen levels were found to be increased 30 days before birth and remained at the same level for the whole 12 weeks of follow-up in male parents. Thus, the higher levels of estrogen in men are probably responsible for more nurturing behavior in new fathers. Furthermore, results showed that prolactin levels rose by approximately 20% in men during the 3 weeks in the postpartum period. Moreover, men who expressed the greatest desire to comfort the crying baby were shown to have the highest prolactin levels and the greatest reduction in testosterone. Additionally, higher cortisol levels were detected in both parents after childbirth. Thus, the study implicated that men probably have similar stage-specific differences in hormone levels as women including higher concentrations of prolactin and cortisol after childbirth and lower postnatal concentrations of testosterone and estradiol. [25] Gordon et al. studied plasma prolactin and oxytocin levels of 43 male parents at the second month and sixth month in the postpartum period. Moreover, the relationship between paternal prolactin and oxytocin profile and child-father interaction in a social context was evaluated. Prolactin and oxytocin levels showed high individual stability across time and each of these hormones was found to be correlated with a specific aspect of paternal behavior. Prolactin was found to be associated with father-infant exploratory play in a social context, whereas oxytocin was found to be related to father-infant affect synchrony during social play. Thus, the results indicated that prolactin and oxytocin probably have a crucial role in the development of paternal behavior in humans. [3] Gettler et al. studied the prolactin blood levels of new fathers and compared the values with those of male partners of the same age who were not fathers. The results indicated that fathers had higher prolactin levels than male partners who were not parents. Moreover, higher prolactin levels were measured in the blood samples of fathers of infants in comparison with fathers of older children. [24] Fleming et al. evaluated plasma prolactin concentrations as well as salivary testosterone and cortisol levels prior to and after the crying of the newborn in order to determine the responsiveness of new fathers and nonfathers toward infant cues. They found that fathers with higher, as opposed to lower, prolactin levels were more alert and more responsive to the baby's cries. Moreover, fathers and nonfathers who had lower testosterone levels were more sympathetic and responsive to the infant's cries. The researchers concluded that similar to a number of other biparental species, human fathers were more responsive to infant cues than nonfathers and this was most probably due to both hormones and caregiving experiences. [26] Moreover, Gettler et al. investigated the effects of paternal care on hormones. In other words, they evaluated the hormonal responses of fathers after interacting with their offspring. Testosterone, cortisol, and prolactin levels in the saliva and plasma were studied at the baseline and 30 min and 60 min after child-father interaction. The results indicated that prolactin profile declined from the baseline after paternal behavior. Fathers who spent more time in daily caregiving and men who thought their spouses evaluated them positively as parental caregivers experienced a larger decline in prolactin levels in comparison with other male parents. Moreover, first-time fathers had a larger decrease in both prolactin and cortisol levels in comparison with experienced fathers. Moreover, testosterone levels did not show a variation at the baseline and after father-infant interaction. Thus, a psychobiological connection between men's perceptions of themselves as fathers and their hormonal responsiveness to parental care was suggested. [51] Discussion Social bonds and affiliations in humans develop within a matrix of biobehavioral attunement. [23] Indeed, the significant role of parental love and care-giving as an incentive force for developmental processes and as a delicate element of survival, safety, and well-being of the young cannot be denied. [56] The findings of studies on hormonal bases of paternal care in nonhuman animals yielded a rich source of hypotheses for studying paternal behavior in humans. [57] Studies on nonhuman mammalian species and emerging data in humans suggest that the formation of paternal care as well as maternal behavior is regulated by neuroendocrine mechanisms in which prolactin plays an integral role and lays the foundation for the development of future social and emotional competencies. According to the available clinical studies, elevation in the amount of prolactin level after childbirth in male parents is probably associated with paternal behavior observed in humans. [3],[24],[25],[26],[58] Additionally, a decline in the testosterone level in male parents after childbirth was observed. [25],[26] Moreover, the prolactin level was found to be correlated with father-infant interaction in a social context, and fathers with higher prolactin profiles were found to be more responsive to baby cues. [25],[26],[58] Additionally, elevated paternal prolactin levels after the birth of the infant probably not only induce parental behavior over time but also decrease the parents' libidos. In this way, parents are probably more involved in parental care and their fertility behavior is reduced. This happens in the context of child-rearing and facilitates behavioral and emotional states associated with successful infant care. Indeed, neuroendocrine mechanisms and behavioral expressions establish the way individuals function in social relationships later throughout their lives. [23] According to a 30-year longitudinal study, appropriate caregiving in infancy and childhood predicted better future social adaptation, emotional regulation, social competence, and more secure romantic relationships. [59] Thus, it can be argued that beyond each physiological mechanism lies a level of wisdom, known as well as yet to be discovered, which encompasses all science and intrigues scientists time and again. To our knowledge, the current study is the first to review the regulatory role of prolactin in paternal behavior in humans and nonhuman mammalian species. Since clinical studies were limited in number, much further research is required to provide a conceptual framework for establishing neuroendocrine underlying of paternal behavior in human male parents. Moreover, the available clinical studies relied on peripheral measures of prolactin in the plasma and saliva. Thus, the inability to directly measure prolactin at the brain neurochemical level presented a limitation. Hopefully, molecular measurement techniques in the future will enable researchers to overcome such obstacles and give a more clear picture regarding neuroendocrine correlates of affiliative behavior and social bonds. Furthermore, measuring all the hormonal levels of estrogen, testosterone, oxytocin, vasopressin, and glucocorticoids at the baseline and different time intervals in the postpartum period is suggested for further research. Financial support and sponsorship Financial support was solely provided by the authors. Conflicts of interest There are no conflicts of interest.[60]
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