How Mothers Are Born: A Psychobiological Analysis of Mothering
A quick scan of how mothers engage with their infants and how they feel about it indicates just how variable mothering is – some mothers talk to their infants, while others sing, stroke and cuddle, and disattend, and, sadly, will neglect or be harsh with them. Although “responsive” maternal behavior enhances the fitness of the mother by ensuring the survival and reproductive efficacy of the offspring, this broad “phenotype” is not a unitary construct, controlled by a single endocrine or brain system, but instead comprises multiple behavioral systems, each with its own neural, endocrine, and behavioral profile. The quality of mothering shown by a new mother depends on her experiences with infants while growing up, her stress level, her affective state, her attention and executive function, how her perceptual systems are tuned, the salience to her of infants and infant-related cues, and how rewarding she finds her interactions with her infant. These behavioral systems are affected by circulating hormones and are mediated by an equally complex set of brain systems with their own neurochemistries and sensitivities. These systems in turn have developed as a function of mothers’ genetics and early experiences in the family of origin. Using both animals and humans as models for one another, this chapter explores this array of interacting factors that contribute to mothers’ responses to their young infants.
KeywordsMaternal Behavior Depressed Mother Maternal Sensitivity 5HTTLPR Genotype Early Postpartum Period
Given the enormous complexity of mothering, it is quite extraordinary that mammalian mothers are generally so adept at raising their offspring. Explaining this by invoking concepts of instinct or innateness is taking the assertion to a different analytic level, one related to concepts of evolution, natural selection, and “fitness.” However, explanations at the level of individual development and proximate mechanism can also be invoked. The focus of this chapter is a description and analysis of this complexity. The behavior of new mothers toward their offspring shows both marked similarities and considerable differences within cultures, across cultures, and certainly across species. The obvious similarities among mammalian species that show mothering include nursing and a posture designed to enhance the neonates’ access to the teat, some form of communication system between mother and offspring to indicate “needs” of both, a way of transporting offspring, especially if they are altricial or immature at birth, and some form of maternal “protective” defense of offspring. Most mothers also keep their offspring clean by grooming and provide a home base or “nest site” either in the environment or on their bodies where the young can sleep. In addition to performing these functions, human mothers also normally develop feelings of nurturance and warmth (or “love”) toward the baby, anxiety in response to distress or unexpected separations from the baby, and grief with his/her loss or death (see Corter & Fleming, 2002; Fleming & Li, 2002; Gonzalez, Atkinson, & Fleming, 2009); see also edited volumes by Bridges (2008) and Bornstein (2002).
The differences among species in the typography, timing, and duration of the behaviors, their developmental trajectory, and the range of proximal causal mechanisms are vast. The differences emerge as a function of the developmental maturity of the young. In most mammalian species, the young are altricial, often born with their eyes and ears closed and with immature nervous systems; these young require extensive care and are very dependent for early survival. Other species are much more mature, or precocial, at birth and are more independent early on (as with ungulates where the young stand within minutes of birth and ambulate behind the mother within days) (Numan, Fleming, & Levy, 2006). Humans are mostly altricial: although they can see and hear at birth, they require a long period of care before they can fend for themselves (some would say this takes two decades or more!!!). Arguably more intriguing – or less well understood – than cross-species differences are individual differences within a species.
In humans, there are both cross-cultural similarities and differences in mothering behaviors. Among the modal similarities are included nursing (Leiderman & Leiderman, 1977), singing (Trehub, Unyk, & Trainor, 1993), and contingent responding to infant distress (Ainsworth, Bell, & Stayton, 1974; Corter & Fleming, 2002; Pederson et al., 1990). However, in the absence of explicit practice, first-time mothers exhibit a range of different responses to their infants: some look at them directly while others gaze avert (Brazelton, 1972); some keep their babies unclothed and stroke their bodies; others swaddle them instead (see Corter & Fleming, 2002). Some talk or sing to their babies; others do not (Tronick, 1987). Some sleep with their babies, while others put their babies in a cot next to them or in their own rooms (see Thoman, 2006). Babies are also transported in different ways – some on the front of the body, others on the back; some on cradle boards and others still, in a vehicle.
More subtly, within a culture mothers show large variations in the postpartum development of nurturant feelings, from minutes to months (Leifer, 1980; Moss & Jones, 1977; Robson, 1967; Robson & Kumar, 1980; Trevathan, 1983) and once “attached” or emotionally committed, in the intensity with which they exhibit different caregiving behaviors. More extremely, some are motivated to provide warmth, shelter, and food to the infant, while others neglect or even abuse their infants (see Corter & Fleming, 2002; Hrdy, 2005, 2009).
In this chapter, we describe the proximal mechanisms regulating the onset, maintenance, and development of mothering, comparing and contrasting two altricial mammals, rat and human, with quite different ecologic constraints and evolutionary histories. Rats are nocturnal, litter-bearers, very immature at birth, rapid developing, short-lived, and have relatively thin nonvariegated cortices reflecting simplicity of cognitive function. In contrast, humans, as we know are diurnal, bearer of singletons or, more rarely, multiples, have a long period of prepubertal development, are long-lived, and have an extensive neocortex and cognitive life (see Numan et al., 2006). The primary goal of this chapter is to unpack the complexity of mothering in rats and humans in terms of the behavioral systems that contribute to individual differences in effective mothering and their distinct and overlapping hormonal, neural, and neurochemical mechanisms. Given the psychobiological approach to mothering that we adopt and the audience for whom this chapter is intended, we emphasize cross-species similarities in organizational principles rather than phenomenologies and mechanisms associated with the obvious differences.
Mothering is not a structure; it is not a reflex; it is not unidimensional. To engage in mothering behavior, mothers have to be sensitive to infant cues and select those cues for processing, utilizing multiple sensory and perceptual modalities; the cues must be attractive and salient for the mother, recruiting reward and approach systems. Mothers must be emotionally prepared and positively motivated to engage socially with the infant, depending on systems regulating affect. They must selectively attend to the offspring in the context of competing stimuli, enacted through systems that regulate attention, and they must be restrained and consistent in their responsiveness, depending on systems that regulate impulsivity. Finally, mothers gain through experiences, acquired both early in life and with young as juveniles and in adulthood. These experiences are acquired, consolidated, and stored as motor or sensory memories and are based on extensive brain plasticity.
In short, to mother appropriately requires the action of multiple behavioral systems in the domains of sensation, perception, affect, reward, attention and executive function, impulsivity, and learning. And then, of course, there is the motor system without which no behavior could occur. This chapter discusses each of these behavioral systems as they apply to rat and human mothers, both descriptively, in terms of the phenomenology and in terms of their underlying hormonal, neural, neurochemical, and genetic regulation. It also discusses some developmental studies that provide clues about how early experiences of being mothered – or not – influence the development of mothering and contributing behavioral and physiological systems. This chapter is not intended to be exhaustive in its scholarship. Instead, it depends heavily on the work our laboratory has done, while attempting to integrate our work with closely related work in the field. Given how extensive the “mothering” field has become, we apologize in advance if we have failed to cite some of the more seminal studies. We are likely to omit many of our own as well.
Psychology of Mothering
Hormonal Background to the Psychology of Mothering
In addition to pregnancy hormones, postpartum hormones from the hypothalamic–pituitary–adrenal (HPA) axis may also play a role in mothers’ response to their newborns. The HPA axis has been studied extensively in relation to reactivity to social, behavioral, and psychological stimuli (Cacioppo et al., 1998; Dettling, Gunnar, & Donzella, 1999; Kirschbaum, Wust, & Hellhammer, 1992; McEwen, De Kloet, & Rostene, 1986; Smyth et al., 1998; Stansbury & Gunnar, 1994). Fleming and colleagues (Corter & Fleming, 1990; Fleming, Steiner, & Anderson, 1987) examined cortisol in relation to maternal behavior in the early postpartum period when cortisol levels are relatively high and mothers’ emotional status is labile. The latter studies indicate that higher cortisol levels on days 3 and 4 postpartum were significantly and strongly associated with maternal approach behaviors, positive maternal attitudes, or more vocally active infants.
Rat pups and human infants represent a constellation of olfactory, auditory, and visual cues that orient, arouse, and direct mothers’ attention. These cues are of special salience to mothers, compared with nonmothers. This salience can occur prior to extensive contact with the young, under the influence of the parturitional hormones, but is definitely enhanced by actual experiences interacting with the young (Fleming et al., 1993; Fleming, Steiner, & Corter, 1997; Orpen & Fleming, 1987; Schaal & Porter, 1991).
An example of stimulus salience in the olfactory domain is presented in a study in which new postpartum rat dams (mothers) and same-aged nonmother virgin females were compared for duration of sniffing of woodchips used as nesting material by a lactating female and her pups, and of woodchips used as nesting material by a nonlactating female. New mothers showed a clear preference for the lactating/pup nest material, whereas the nonlactating female showed no preference, indicating that the odors associated with lactation and pups are positive and salient to the postpartum animal (Fleming, Cheung, Myhal, & Kessler, 1989). That this preference was not primarily the result of the actual experience of the odor of lactation and pups is indicated by a follow-up study showing that a similar preference for the lactating/pup odors was found among virgin animals who had received hormonal priming that mimics the hormonal changes associated with later pregnancy and parturition that are normally experienced in the new parturient mother (Fleming et al., 1989).
Using an analogous procedure, similar results were found among populations of human mothers. Fleming et al. (1993) asked groups of mothers of 2-day-olds, 1-month-olds, and female and male nonparent controls to rate the pleasantness of a variety of infant-related and noninfant odorants. Odors consisted of 2- to 3-day-old infant t-shirts (worn for 8–12 h), infant urine, infant feces, adult axillary odors, spice, and cheese. The primary findings show that new mothers give higher hedonic ratings to the infant t-shirts than do nonmothers, while not differing in response to other stimuli. Mothers who give positive ratings experienced, on the one hand, a shorter postpartum interval to the first extended contact and nursing of their infants and, on the other hand, a heightened maternal responsiveness, measured both behaviorally and by self-report. Based on these findings, it seems that new mothers show heightened attraction to the general body odors of infants, but this attraction varies as a function of early postpartum contact and experiences interacting with young.
In addition to experience, the postpartum hormone cortisol influences responses to newborn baby odors (Fleming, Steiner, et al., 1997). In general, associations between cortisol and hedonics are found only in primiparous mothers: higher levels of cortisol predicted higher ratings of infants’ t-shirt body odors and urine but were unrelated to control odorants (Fleming, Steiner, et al., 1997). Maternal report of greater prior experience with infants also predicted higher ratings. These patterns suggest that both cortisol and experience are tied to attraction to infant odors and further suggest that prior experience could mask hormonal effects on attraction since they were seen only in first-time mothers. In addition, there was a positive correlation between cortisol levels and the success at recognizing one’s own infant, but only for multiparous mothers (Gonzalez, Jenkins, Steiner, & Fleming, 2009).
Mother rats are also selectively responsive to their offspring’s vocalizations, which when presented in combination with pup olfactory cues elicits selective orientation and approach. The same is true for hormonally primed nonmothers by not for nonhormonally primed animals (Farrell & Alberts, 2002). Human mothers are also very responsive to infant vocalizations, especially their cries (Stallings, Fleming, Corter, Worthman, & Steiner, 2001). Mothers, but not nonmothers, experience elevated levels of sympathy and alertness in response to cries of babies but not in response to white noise. Moreover, as with odor responsiveness, the extent of sympathy experienced by mothers uniquely is related both to mothers’ cortisol levels and to her heart rate (Stallings et al., 2001). Mothers with higher circulating levels of cortisol and higher baseline heart rates (prior to stimulus presentation) tend to respond more sympathetically when they hear the infant cries (Stallings et al., 2001). The positive association between cortisol levels and sympathetic responses is consistent with our earlier findings of a positive association between cortisol and positive responses to infants and infant odors in new mothers (Fleming, Steiner, et al., 1997). In the Stallings et al. (2001) study, mothers with higher baseline cortisol levels also showed greater sympathy to pain cries and less sympathy to hunger cries than did mothers with lower cortisol. Furthermore, mothers with higher baseline cortisol levels also had higher baseline heart-rate responses, and both physiological measures showed a similar relation to sympathetic feelings. In contrast to the patterns of individual differences, there was little evidence of differential infant stimulus effects. That is, there were no differences in either hormones or heart rate in responses to cries vs. odors. In fact, hormones underwent very little change with either stimulus. Thus, individual differences in maternal physiology, perhaps as part of personality differences, seem to play a major part in affective responses to infant stimuli.
Finally, unlike most animals that have been studied soon after birth, humans are strongly visual animals and mothers are adept at recognizing the face of their own newborn from a set of infant pictures (Kaitz, Good, Rokem, & Eidelman, 1988; Kaitz, Rokem, & Eidelman, 1988). A study by Wiesenfeld and Klorman (1978) demonstrated physiological arousal effects for parents at the sight of their own baby crying or smiling; heart rate (HR) first decelerated and then accelerated as parents viewed silent videotapes of their 5-month-old infants. Leavitt and Donovan (1979) found that mothers of 3-month-old infants responded with HR acceleration when the gaze of an unfamiliar infant was directed toward them but did not display this arousal pattern when the infant was looking away. At the behavioral level, the infant’s gaze appears to evoke mother’s gaze (Messer & Vietze, 1984) and thus lead to “en face” behavior between the two, which Klaus, Trause, and Kennell (1975) have described as species-typical maternal behavior. These and other studies (Butterfield, Emde, Svejda, & Naiman, 1982; Stern, 1974; Trevathan, 1987) indicate that infant visual stimuli are powerful stimuli for the elicitation of maternal behavior and are clearly important in the sequence of interaction between infant and mother.
Taken together, these results suggest that like a number of other species in which infant odor attraction contributes to mothers’ early attachment to their offspring (Levy, 2008) and mothers are sensitive to the distress vocalizations of their infants, human mothers find infant-related odors to be attractive and cries to be salient. These perceptions are affect-laden and related to hormones and enhanced by experience. They also have motivational properties (Bridges, 2008; Fleming, Gonzalez, Afonso, & Lovic, 2008).
Affect and Attention
Once mothers have become maternal or become “attached” to their infants, the ways in which they interact with their infants also show significant individual differences, and these differences reflect differences in mothers’ mood, attentional capacity, impulsivity, and ability to learn about their infants and about mothering.
The postpartum period is a period of huge endocrine upheaval. The hormonal shifts that occur at this time are among the greatest in any time in a female’s life. Although, as we have seen, the specific hormones may vary, in both rats and humans they act not only to alter perception; they also function to modulate mothers’ affect, which in turn influences behavior. In rats, this affective change takes the form of a change along the activity and fear dimensions. In humans, it is along the depression dimension.
When placed into an open-field apparatus used to assess activity and “anxiety,” new mother rats and hormonally primed rats exhibit hyperactivity and reduced neophobia in response to a novel object (Fleming et al., 1989; Fleming & Luebke, 1981) in comparison to virgin nonmothers, as reflected in the proportion of activity spent in the center as opposed to the periphery of the field and time spent sniffing a novel object. Similar effects are found using other measures of anxiety (the elevated plus maze) (Neumann, Wigger, Liebsch, Holsboer, & Landgraf, 1998). Under the influence of the parturitional hormones, new mothers are less neophobic and, hence, less avoidant of pups than are nonmothers (Fleming & Luebke, 1981). Drugs or manipulations that reduce the neophobia in virgins also have the effect of facilitating maternal responding to foster pups in virgin animals that are normally not maternally responsive to pups (Hansen, Ferreira, & Selart, 1985; Mayer, 1983).
Among humans, the most notable change that a new mother undergoes with the birth of a baby is in her mood. A high proportion of mothers experience what has come to be known as the “postpartum blues” and also heightened lability within the first postpartum week (ca. 26–85%, depending on the diagnostic criteria; Bright, 1994; Gold, 2002; O’Hara, Zekoski, Philipps, & Wright, 1990); a small but substantial percent of women also experience more severe dysphoria and postpartum depression (PPD) that extends past the first few weeks, although it usually remits by 5 months postpartum (Cooper & Murray, 1995; Cox, Connor, & Kendell, 1982; Cox, Murray, & Chapman, 1993; Gold, 2002; Stowe & Nemeroff, 1995). The symptom profile of PPD resembles that of a major depressive episode experienced at other times in life, including fatigue, negative affect, negative thoughts, suicidal ideation, and low self-esteem (Beck, 2002; Gold, 2002; Seyfried & Marcus, 2003; Wisner & Stowe, 1997), but it is unique in its timing, always involving at least the mother–baby dyad and in most cases an entire family unit.
Although it is widely believed that these mood changes are hormonally mediated, there is considerable debate in the literature as to the causes of this clinical condition (e.g., Ross, Sellers, Gilbert Evans, & Romach, 2004; Steiner, 1998). What is clear, however, is that dysphoric women often have difficulty interacting with their infants. Although depressed mothers do not report feeling less attached to their infants (Fleming, Ruble, Flett, & Shaul, 1988), and in fact may show considerable warmth and interest (Stein et al., 1991), depressed mothers respond less sensitively and more negatively to their infants than do nondepressed mothers (Cohn, Campbell, Matias, & Hopkins, 1990; Field, Healy, Goldstein, & Guthertz, 1990; Fleming et al., 1988; Murray, Fiori-Cowley, Hooper, & Cooper, 1996; Stanley, Murray, & Stein, 2004). At 2 months postpartum, their speech contains more negative affect, and in play interactions they exhibit fewer responses to the infant’s behavior (Murray et al., 1996). During face-to-face interactions with their infants, depressed mothers are also more prone to exhibit controlling, intrusive, and overstimulating behavior, or withdrawal, passivity, and disengagement (Cohn et al., 1990; Field et al., 1990; Lovejoy, Graczyk, O’Hare, & Neuman, 2000; Malphurs, Raag, Field, Pickens, & Pelaez-Nougeras, 1996). Moreover, when observed interacting with their infants they tend to spend less time than nondepressed mothers engaging in behaviors that “match” the behaviors of their infants and more negative states were matched (Field et al., 1990). Similarly, other studies have found that the depressed dyad presents fewer vocalizations and fewer visual communications; at 6 months postpartum, they use less affective and less informative speech, and their overall level of tactile interaction behavior is lower (Fleming et al., 1988; Herrera, Reissland, & Shepherd, 2004; Righetti-Veltema, Conne-Perreard, Bousquet, & Manzano, 2002).
Although the literature indicates that depression itself also predisposes people to problems with attention, to date no studies relate PPD to inattention in new mothers. There are also no studies on attentional or impulsivity changes associated with parturition in rats; preliminary studies in humans do not show that new mothers are more generally attentive, using the Cambridge Neuropsychological Test Automated Battery (CANTAB) (Sahakian et al., 1988), than are nonmothers (Chico, Ali, Eaton, Gonzalez, & Fleming, in preparation). However, there is considerable evidence that general (nonspecific) attention (and perhaps impulsivity) is related to quality of mothering (Gonzalez, Jenkins, Steiner, & Fleming, submitted). In animal studies, mother rats who show reduced selective attention using an animal version of an attention test normally administered to human subjects (the Wisconsin card sorting task) and reduced sensorimotor gating (an “automatic” startle-attention task, prepulse inhibition test) also show reduced crouching behavior and licking of the young (Lovic & Fleming, 2004). Tests of motor impulsivity similarly indicate a strong inverse relation between motor impulsivity and mothering behaviors (Lovic et al., 2010), suggesting that these general behavioral systems must be working optimally for adequate maternal behavior to occur. In humans, as well, we now know that attention is related to sensitive mothering.
It is often difficult to ascertain how rewarding the young are to the new mother. However, when deprived of young for a period, new rat mothers will bar press in an operant box adapted to deliver pups with each bar press (Lee, Clancy, & Fleming, 2000). Nonmothers will not. Also, rat mothers develop conditioned place preference for chambers that have been associated with pups, whereas nonmothers tend to avoid those chambers (Magnusson & Fleming, 1995), suggesting a difference between the two kinds of animals in the rewarding properties of pups. More impressively the, work by Morrell and colleagues (Mattson, Williams, Rosenblatt, & Morrell, 2001; Seip & Morrell, 2007; see Pereira, Seip, & Morrell, 2008) shows that when given a choice between a chamber that has been associated with pups and one associated with cocaine, soon after parturition new mothers will prefer the pup-associated chambers, whereas later in the postpartum period, as weaning is occurring, the preference shifts to the cocaine-associated chamber (Mattson et al., 2001; Seip & Morrell, 2007). The reward value of young has not been studied in the same way in humans, but there is no question that with experience new mothers spend increasing amounts of time talking about infants, often at the expense of apparent interest in the partner – an effect that reverses itself toward the end of the first postpartum year, possibly in preparation for the initiation of a new maternity cycle!
Young must have rewarding properties to help sustain maternal motivation and responsiveness and to insure long-term maintenance of interest in young. A substantial literature shows that new mothers learn about their offspring and they do this relatively easily. In a series of studies on the maternal experience effect, Bridges (1975) as well as Fleming and her colleagues (see Fleming & Li, 2002) have explored the situational and sensory factors contributing to this learning. Summarizing an extensive behavioral literature, it is clear that as little as half an hour of interactive contact with young after their birth is adequate to sustain some level of maternal responsiveness for many days, in the absence of the continued presence of pups. The nature of the experience is, however, important. If, during the interactions, the mother cannot smell the young (Fleming, Gavarth, & Sarker, 1992; Mayer & Rosenblatt, 1977) or cannot experience somatosensory input on the ventrum after an anesthetic is applied, this responsiveness is sustained less well (Jakubowski & Terkel, 1986; Stern, 1983). Moreover, simple exposure to pup-related odors, or visual and auditory cues, is not adequate to sustain the responsiveness to pups (Morgan, Fleming, & Stern, 1992). Apparently for robust learning to occur, mothers must actively interact with the pups and receive sensory input during that interaction (Morgan, Watchus, Milgram, & Fleming, 1999). A similar situation occurs in many other mammalian species, especially in ungulates where individual recognition of individual offspring (unlike rats which recognize litters but not individuals in a litter) is essential to prevent the ewe from rejecting the young altogether. In the case of these species, the learning is clearly olfactory based and is rapid and enduring (see Numan et al., 2006).
In humans, individual recognition of the infants’ odors as well as the infants cries and the tactile characteristics of the hand also occur (see Corter & Fleming, 2002; Kaitz, Good, Rokem, & Eidelman, 1987; Kaitz, Lapidot, Bronner, & Eidelman, 1992; Porter, Cernoch, & McLaughlin, 1983). Recognition is based on experience with the infant and also occurs in the first few days of the infant’s life (see Corter & Fleming, 2002). In addition to this kind of sensory learning among humans, experience interacting with the infant at birth and after birth enhances the mothers’ feelings of competence and self-esteem, which affects her subsequent interactions with her baby (e.g., Thompson, Walker, & Crain, 1981). In fact, there is an extensive disputed literature on early postpartum learning by the mother, where researchers in the 1970s claimed that human mothers also have a critical period in which to interact with the baby in order for appropriate attachment to occur (e.g., Klaus and Kennell, 1976). This claim has continued to be debated, with some recent indications that aspects of maternal behavior and infant development may in fact be correlated with an early postpartum period of contact between infant and mother (Bystrova et al., 2009); however, other studies have indicated no adverse effects on mother’s attachment of separation from the baby at this time (see Moore, Anderson, & Bergman, 2007).
The role of hormones in the early postpartum learning, while clearly demonstrated in sheep (Numan et al., 2006) and possibly even in rats (Numan et al., 2006), seems not to be the case in humans – as far as we know.
Taken together, behavioral studies suggest that the onset of mothering at parturition and its expression during the early postpartum period depend on appropriate activation or functioning of systems that we believe are essential for mothering, including systems associated with perception, affect, attention, reward, and learning. Changes in all these systems occur at the time of birth. Where we have explored it, they are enhanced or modulated by the parturitional and postpartum hormones, established either experimentally as in the rat model or through a correlational approach in humans.
The Physiology of Mothering
Neuroanatomy of Maternal Behavior
Through extensive work produced by a number of laboratories, the neural circuitry underlying the onset and expression of maternal behavior in rats is well delineated. In summary, there seem to be three primary systems that intersect and that are activated by pups and by hormones in the maternal rat.
Perceptual System Intersecting with the Emotion System
The Final Common Path for Maternal Behavior
The second system that constitutes the “final common path” for the expression of the behavior includes the medial preoptic area/ventral bed nucleus of the stria terminalis (MPOA/vBNST) and its downstream projections into the midbrain [ventral tegmental area (VTA)] and hindbrain [periaqueductal gray (PAG)] and sensory, limbic, and cortical systems that project into the MPOA/-vBNST. The MPOA contains receptors for all the hormones involved in the activation of maternal behavior, including receptors for estradiol, progesterone, prolactin, oxytocin, vasopressin, and opioids (Numan & Insel, 2003; Numan et al., 2006). Lesions to the MPOA eliminate most maternal behaviors in the postpartum rat, and electrical or hormonal stimulation of this group of neurons activates or facilitates maternal behavior in nonmaternal animals (Bridges, 2008; Numan et al., 2006).
Afferents to the MPOA from Systems Mediating Reward, Emotion, Attention and Memory
Neurons projecting into the MPOA are involved in many of the other behavioral changes described above, including changes in mothers’ affect [AMY orbitofrontal, prefrontal (mPFC) and anterior cingulate cortices (ACC)], sensitivity to stimulus salience [(AMY) and to reward striatum/nucleus accumbens (NAC)] as well as attention (NAC, mPFC), and memory (NAC, mPFC). Some of these brain sites also contain hormone receptors (AMY, mPFC) and may be the sites where the periparturitional hormones act to change behavior at the time of parturition (Numan et al., 2006). The relatively complicated neuroanatomy of maternal behavior is based predominantly on work with rats, voles, sheep, and primates (Bridges, 2008; Numan et al., 2006). Taken together, these cross-species studies indicate a striking similarity in the neuroanatomy that underlies mothering.
Work on neural bases of maternal behavior in humans is derived primarily from approximately ten fMRI studies where mothers, nonmothers, and sometimes fathers are presented with either pictures of their own infants or same-aged unfamiliar infants (Bartels & Zeki, 2004; Leibenluft et al., 2004; Nitschke et al., 2004), recorded infant cries (Lorberbaum et al., 2002; Seifritz et al., 2003), or videotapes of infants (Ranote et al., 2004). All studies demonstrate that many of the same hypothalamic, limbic, and cortical sites important for emotional or social (face) processing or for regulation of maternal behavior in other mammals are implicated in response to infant stimuli. Although promising, these fMRI studies are still few in number, often with small sample sizes and great variation in methodology, including age of infant/child tested, use of own vs. other infant/child as experimental stimuli, use of control stimuli, and stimulus matching-standardization procedures.
We have been investigating the neural response to positive and negative infant faces in non-PPD mothers at approximately 3 months postpartum (see Barrett et al., 2010). Analyses of face ratings in our current fMRI study (data from 18/23 moms) revealed that in response to own compared to other positive infant faces, mothers reported feeling significantly more alert, calm, delighted and interested as well as experiencing a greater “need to respond.” Interestingly, no significant differences were found for the negative faces. We have also found that, compared with viewing other positive infant faces, viewing own positive infant faces was associated with increased brain activation in the anterior cingulate cortex and regions of the medial prefrontal cortex (PFC). Our behavioral and neuroanatomical results suggest that viewing own positive infant faces was more salient for mothers and resulted in greater activity in reward/emotion and possibly, mothering-related brain regions.
Neurochemistry of Maternal Behavior
The importance of the MPOA, NAC, and mPFC in the expression of maternal behavior, pup reward, emotion, and attention points to the importance of a number of neurotransmitter systems that promote communication among these sites and that are important for the motivation and expression of maternal behavior. Although there are a number of relevant neuropeptides and neurotransmitters (serotonin, dopamine, glutamate, GABA, oxytocin, etc.), here we discuss one primary one on which we have worked extensively. This is the dopamine system.
Dopamine is a neurotransmitter that is synthesized in the VTA and is released through projections into the dorsal striatum (nigrostriatal system), the ventral striatum or NAC and AMY (mesolimbic dopamine system), or the cingulate cortex and medial and orbitofrontal prefrontal cortices (mesocortical dopamine systems). The systems of most interest in the present context are the mesolimbic and mesocortical systems, which function in the mediation of reward, stimulus salience, and attention (Berridge & Robinson, 1998). In terms of dopaminergic effects on maternal behavior, there is now substantial literature showing that dopamine receptors in the NAC are activated by pups; systemically administered DA receptor antagonists disrupt pup approach and retrieval in mother rats (Hansen et al., 1985; Li, Budin, Fleming, & Kapur, 2005; Li, Davidson, Budin, Kapur, & Fleming, 2004; Numan et al., 2005; Parada, King, Li, & Fleming, 2008) and when infused directly into the NAC, they block both retrieval responses (Li & Fleming, 2003a, 2003b; Numan et al., 2005; Stern & Keer, 1999) and consolidation of experiences with the offspring acquired by the mother postpartum (Li & Fleming, 2003a, 2003b). Conversely, infusion of DA receptor (DRD1) agonists into the NAC enhances maternal behavior (Numan et al., 2005).
In a follow-up series of studies in our laboratory, Afonso and colleagues (Afonso, Grella, Chatterjee, & Fleming, 2008; Afonso, King, Chatterjee, & Fleming, 2009) have explored the pattern of dopamine release within the NAC in response to pups and food in new recently parturient mothers, in females that are not postpartum but are maternally experienced, in virgin females, in virgin females administered parturitional hormones, and in females that were reared without their own mothers. New mothers show a robust sustained dopamine response to pups whereas virgin nonmothers do not; both show an acute response to food. Hormonal experience contributes to this mother effect since if virgins are administered the hormones by means of silastic capsules and are presented with pups, they too show a robust dopamine response to pups, even if they are not yet maternally interactive with them (Afonso et al., 2009). However, although hormones augment dopamine responsiveness they are not necessary to the dopamine response, since multiparous animals that are not postpartum, but are cycling, when given pups, also show elevated dopamine in response to pups (Afonso et al., 2008). In this case, however, the dopamine response is more acute and less sustained.
The additive effects of experiences being maternal has also been demonstrated, where multiparous animals reinduced to be maternal through sensitization or continuous exposure to pups show a greater dopamine response to pups than do multiparous animals not recently exposed to pups; both show higher DA responses than do virgin animals induced to be maternal through pup exposure (Afonso et al., 2008). However, all maternal groups have higher extracellular DA levels than do inexperienced virgins. Although on first glance the results appear somewhat complicated, if one equates dopamine release in this context with reward (and that is, of course, a disputable assumption!), then these studies suggest that both the hormones associated with parturition and prior experiences interacting with pups confer on the pups reinforcing properties, and animals experience pups as rewarding stimuli. If one were to prioritize experiences in terms of the rewarding value of pups (using DA here as that measure), it appears that effects are additive: pups are most rewarding to the female who has been exposed to both hormones and experience, followed by experience alone or by hormones alone. However, if mothers are raised without mothers but on an artificial feeding regimen, their later maternal behavior is disrupted as is their preference for pup cues. Moreover, in this situation DA is still released in response to pups but to a considerably reduced extent (Afonso, Burton, Nabakov, & Flerming, in preparation).
Animal models clearly provide evidence for biological and neuroendocrine substrates behind the regulation of maternal behavior. A logical question is whether these substrates and subsequent behaviors have a genetic component. In mice, knockouts in genes relating to endocrine function (oxytocin, CRF – e.g., Gammie, Bethea, & Stevenson, 2007; Pedersen, Vadlamudi, Boccia, & Amico, 2006), as well as strains with disrupted serotonergic signaling (Lerch-Haner, Frierson, Crawford, Beck, & Deneris, 2008), show disruptions in maternal behavior. Using microarrays to determine the pattern of gene expression during the exhibition of maternal behavior, we have found that many categories of genes are expressed at parturition. These include genes associated with general metabolism, brain plasticity, steroid hormones, multiple enzyme systems, and selected neurotransmitters. However, of particular interest in the present context are the dopamine and serotonin genes as well as genes associated with endocrine changes of parturition. Preliminary analyses indicate that within the medial preoptic area (MPOA), a number of genes for dopamine receptors show differential expression between virgin and postpartum animals and between groups exposed to pups and those not exposed (Kent et al., in preparation). Using gene expression microarrays to screen for transcripts of a variety of dopamine-related genes, Akbari et al. (in preparation) found that in comparison to non pup-exposed groups, postpartum and virgin maternal animals showed a greater expression of some of the dopamine receptors and the dopamine transporter (DAT) gene. Expression levels for some of these dopamine-related genes were also correlated with hedonic behaviors, especially between DRD4 and sucrose intake and pup retrieval.
In another program of research on rats where we are exploring single neucleotide polymorphisms (SNPs) in selected candidate genes, we have found that at least one dopamine gene, the dopamine 2 receptor (DRD2) gene is polymorphic (with three variants or “triallelic”) at a particular locus on the gene. Moreover, we are finding that the density of dopamine receptors in the NAC is affected by one particular variant of the DRD2 gene (Belay et al., 2010) and an interaction is occurring between this gene and early environment in the density of D2 receptor binding in the accumbens region. Animals with one of the DRD2 genotypes, if raised in a deprived environment, show lower dopamine receptor density than those raised in a normal environment. Environment has no impact on receptor density in the NAC in animals carrying the alternate genotype (Lovic et al., 2010). Whether these gene by environment interactive effects on dopamine physiology translate into effects specifically on maternal reward, hedonics, and mothering in the rat, we do not yet know.
However, thanks to advances made by the Human Genome Project, we are beginning to understand some of the genetics that underlie some of the psychological mediators or modulators of mothering. That some aspects of maternal behavior (e.g., warmth, positivity, physical affection, and control) are heritable was first indicated by twin studies (e.g., Harlaar et al., 2008; Neiderhiser et al., 2004). Recent molecular genetic work examining the dopamine, serotonin, and oxytocin systems also suggests that maternal genotype may predict maternal behaviors. For example, variation in the dopamine transporter (DAT1) gene is associated with differences in the frequency of maternal verbal commands (Lee et al., 2008), whereas catechol-O-methyltransferase (COMT) and DA receptor 4 (DRD4) alleles associated with less efficient transmission predict decreased maternal sensitivity in mothers with high levels of self-reported daily hassles (van Ijzendoorn, Bakermans-Kranenburg, & Mesman, 2008). Also, mothers with less efficient alleles in the serotonin transporter (5HTT) and oxytocin receptor (OXTR) genes are less sensitive in their interactions with their infants (Bakermans-Kranenburg & van Ijzendoorn, 2008).
A multi-systems approach to mothering can partially illuminate these findings, as well as target additional candidate genes by considering systems involved in maternal affect, attention, and cognitive function, all of which are involved in mothering.
Genetics and Maternal Affect
Genetics and Maternal Attention
As indicated above, there is evidence that attentional mechanisms in humans are central to maternal sensitivity (Gonzalez, Steiner, & Fleming, in preparation), and the logical question which is yet to be addressed is whether genetic predictors of human attentional characteristics are also associated with differences in maternal sensitivity.
The DA system helps regulate executive functions and attention, but molecular genetic studies have focused primarily on disorders like attention deficit/hyperactivity disorder (ADHD) and much less on normal variation of dopamine function in nonclinical adult populations. For example, the DRD4 ExonIII 7-repeat polymorphism is an established predictor of ADHD in children, and it is associated with brain morphological differences in ADHD adults (Monuteaux et al., 2008). Polymorphisms in the dopamine transporter (DAT1) and COMT genes are associated with differences in cognitive function, as well as prefrontal activation (e.g., Caldu et al., 2007). Thus, genetic differences that predict cognitive and attentional differences might also be associated with maternal behavior differences.
In adults, the 5HTTPR polymorphism also interacts with adverse life events on ADHD severity (Muller et al., 2008). It is not clear if these polymorphisms are associated with attention or executive function in nonclinical populations, and this has never been assessed in mothers.
Genetics and Hedonics/Reward
New mothers develop an attraction to infant cues and these become rewarding. It is well established from animal literature that the dopamine system is involved with regulating maternal hedonics and maternal behavior, and that dopamine transmission outside of a normal range is associated with deficits in the initiation and consolidation of maternal behavior (Numan et al., 2005, 2006; Parada et al., 2008). The dopamine system is an integral component of reward processing, but most of the molecular genetics studies have examined genetic predictors of neuropsychopathologies in the reward system, including impulsivity, addiction, and gambling. In a study of genetic variation on nonpathological reward system function, Dreher, Kohn, Kolachana, Weinberger, and Berman (2009) found that polymorphisms in two DA-system genes, DAT1 and COMT, were associated with interindividual differences in activation of brain regions involved in reward processing and anticipation, including the ventral striatum and PFC.
Genetics and Hormones
There is evidence that maternal hedonics and sensitivity is related to both cortisol (positively in the early postpartum period; see Corter & Fleming, 1990, 2002; Fleming et al., 1987; Fleming, Steiner, et al., 1997) and depression (Fleming, Steiner, & Gonzalez, in preparation). Predictably, depressed persons have higher cortisol (Gillespie & Nemeroff, 2005). Serotonin system gene polymorphisms (especially 5HTTLPR) moderate the role of stress in the development of depression. One such interaction might be through the role of the polymorphism val/met (MAOA VNTR) in HPA-axis reactivity to psychological and endocrine challenges (Gotlib, Joormann, Minor, & Hallmayer, 2008; Jabbi, Korf, Ormel, Kema, & den Boer, 2008). Another study reports that 5HTTLPR is associated with elevated waking cortisol in girls as young as 9 years of age (Chen, Joormann, Hallmayer, & Gotlib, 2009). If this polymorphism is associated with life-long cortisol profiles, then it might also be important for maternal behavior, in both depressed and nondepressed mothers. It is unclear if genetic variation associated with these underlying differences in mood and endocrine profile is associated with maternal behavior in a predictable way.
We are currently investigating genetic variation in dopamine (DA) and serotonin (5HT) genes in new mothers, as part of a larger study on maternal adversity, vulnerability, and neurodevelopment (MAVAN). The study follows a longitudinal sample of 250 women, recruited at pregnancy and followed until at least 4 years postpartum. We have targeted several DA candidate genes for our association analyses, and preliminary findings indicate that there are some gene–environment effects on the outcome of maternal sensitivity, as measured by the Ainsworth Maternal Sensitivity Scales (Ainsworth, Bell, & Stayton, 1971; Ainsworth et al., 1974) (Fig. 1.4a). Specifically, a DA receptor 1 (DRD1) polymorphism, rs265976, appears to interact with early life adversity, as measured by the Childhood Trauma Questionnaire (CTQ; Bernstein et al., 1994, 2003) to predict level of maternal sensitivity. Mothers who are homozygous for the “G” allele at this locus of DRD1 and who have had a low level of early adversity are more sensitive to their infants during a 30-min mother–infant interaction at 6 months postpartum (Fig. 1.4a). This polymorphism is part of a haplotype (combination of alleles at multiple loci which are usually transferred together) containing three other polymorphisms along the DRD1 gene, and we are continuing our analysis to determine if there are similar associations between haplotypes and maternal behavior that we are seeing with the single polymorphism.
Although the DRD1 receptor is widespread in the human brain, it appears to be particularly abundant in the PFC, striatum, and NAC (Jackson & Westlind-Danielsson, 1994; Missale, Nash, Robinson, Jaber, & Caron, 1998), regions which we know are involved in maternal behavior regulation. In addition, in rat mothers, DRD1 – along with DRD2 – receptors appear to be involved in maternal memory (Parada et al., 2008), and disruptions by antagonists or agonists in the DA system which result in abnormal levels of DA in the maternal circuit also result in disrupted maternal behavior (e.g., Byrnes, Rigero, & Bridges, 2002; Hansen, Harthon, Wallin, Lofberg, & Svensson, 1991; Numan et al., 2006).
Within the serotonin system, which is involved in social behaviors and mood, we began with the 5HTT gene, and asked whether variation in this gene might be associated with differences in maternal behavior. Serotonergic neurons extend from the raphe nucleus of the brain stem into many regions of the brain including the NAC and reward systems. 5HTT has a role in the termination of serotonergic signaling. The 5HTTLPR polymorphism is one of the major polymorphisms on this gene, and it has received much attention for its putative role in the etiology of depression (e.g., Caspi et al., 2003; Risch et al., 2009). The “short” (S) allele at this locus is associated with lower expression of 5HTT mRNA in vitro (Hu et al., 2006), as well as lower 5HTT binding potential in certain human brain regions (Praschak-Rieder et al., 2007). In this way it may serve as an indicator of 5HT turnover, which has in turn been associated with difference in levels of social aggression in humans (e.g., Siever, 2008).
In rhesus macaques, an analogous polymorphism (rh5HTTLPR) has been linked with differences in 5HT metabolites in the cerebrospinal fluid (Cleveland, Westergaard, Trenkle, & Higley, 2004), which further underlines its role in serotonergic turnover. Interestingly, the relationship between this polymorphism and adult 5HT metabolite levels appears to be mediated by early environment; the S allele predicts lower levels of metabolites in peer-raised (early adversity) but not in mother-raised monkeys (see Suomi, 2006). Environment alone also appears to predict differences in serotonergic transmission: peer-raised monkeys have significantly lower 5HTT binding potential (Ichise et al., 2006). Additional studies suggest that monkey maternal behavior may be related to levels of 5HT metabolites, although the direction of this relationship seems unclear (Cleveland et al., 2004; Maestripieri et al., 2006). Nonetheless, these studies highlight the importance of considering both genotype and environment in assessments of subsequent behavior.
By considering genetic factors in analyses that previously relied on other independent variables, we might be able to find effects we have previously discounted. This is particularly true where G × E effects might explain differences in maternal behavior that were not obvious by examining simply environmental effects. For example, as in our case, early adversity may predict that mothers are less vocal when interacting with their infants, but only if the mothers are of a particular genotype. If they have the alternate genotype, early adversity might actually predict increased vocalization and when considered as a function of environment alone, the effect seems to disappear (Fig. 1.4).
Although maternal behavior is crucial for humans and most mammalian species, its onset, maintenance, and variation across and within species is complex and not fully understood. Particularly in humans, this complexity cannot be explained easily and unimodally. Certainly, hormonal, experiential, environmental, sociocultural, and personality factors are involved. Add to that genetic effects, interactions between genes and environment, and perhaps epigenetic modulation – a facet we have not addressed here – and it becomes clear that we are only beginning to understand the underpinnings of this fundamental aspect to mammalian survival.
We have a number of messages we hope to convey in this chapter. First and foremost, we believe that it is helpful to explore cross-species similarities and differences in order at the least to ask biologically relevant questions concerning the etiology of mothering in humans. Second, the analysis of mothering requires an understanding of the regulation of multiple behavioral systems including aspects of perception, emotion, attention, memory, and sensory-motor control. The level of functioning of these systems and their biases impact on mothers’ motivation to mother and her success in mothering. Since we know, for example, that attentional, motivational, and hormonal/physiological neurocognitive components have different and perhaps competing influences on maternal behavior, then we might do better to devise ways of assessing components of observed maternal behavior that are related to each of these underlying components in turn. A videotaped mother–infant interaction coded with an attentional framework in mind might look quite different from one coded with a motivation-related coding schema. Finally, to discuss mothering in humans within a psychobiological context, as we have done here, departs from the usual way of looking at human mothering. By invoking biology, we are in no way eschewing freedom of choice and women’s right to decide about their mothering. It does not mean that somehow mothering is “determined” by biology. Understanding behavior in terms of its psychobiology in fact permits us to understand what factors may be brought into play when choices are made and when infants are born. The new work on genetics and on gene by environmental interactions is a case in point.
Here we have emphasized the similarities between rat and human mothers, in terms of many of the putative proximal regulatory mechanisms. We find that humans, like rats, experience reliable hormonal changes with parturition, which are similar across species. We find that humans, like rats, become attentive to infant cues and become attracted to them with a minimum of interaction with the young. In rats, these changes in hedonic responses are produced by hormones; in humans, they are associated with hormones, albeit different ones! We find in both rats and humans that the quality of mothering is associated with functioning of other behavioral systems. In both, mothering is associated with mothers’ affective or mood state; by mothers’ attention and other measures of executive function; and by mothers’ ability to acquire and retain information, that is, by their plasticity. That these relations are mediated by the same mechanisms in rat and human mothers, in their entirety, is unlikely. That they share some mechanisms in common is likely. We have delineated the neuroanatomy and neurochemistry of mothering in rats, with an emphasis on the mesolimbic and dopamine systems. Recent genetic and fMRI studies suggest a similarity between systems that are activated in rat and human mothers by their offspring. Clearly in humans, other systems relating to earlier experiences, planfulness, executive functions, theory of mind, and cognitions also come into play. The study of many of these very human characteristics and their neurobiology in relation to human mothering is still in its infancy and will provide grist for the mill for many generations of students.
Among the areas that will prove productive are studies relating genetics to epigenetics, using animal models. While there is an emerging literature on epigenetic modulation of maternal behavior as a function of early experience in rats (e.g., Champagne et al., 2008), relating the animal’s genotype and environmental influences to the molecular mechanisms regulating activation of the “maternal” genes has not been done. We would also like to see more studies combining fMRI and other more refined measures of brain activation, in an attempt to reveal the functional neuroanatomy and physiology of human maternal behavior. Finally, there is a huge need to apply research about the role of early adversity and early experiences – and the mediating role of physiological or psychological mechanisms – on later mothering, particularly in high-risk populations, including teenaged mothers or depressed and schizophrenic populations. Related to this is the need to assess rehabilitation and remediation programs for problematic mothering, perhaps targeting problems that might be population-specific. For example, depressed mothers might show patterns of mothering deficits different from those in teenaged nondepressed mothers, and universal remediation approaches might not be appropriate.
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