Brain Circuits for Parental Behavior and Love, with Implications for Other Social Bonds

Share

NumanMichael Numan, Department of Psychology, University of New Mexico

Introduction

January 2016 – Parental behavior can be defined as any behavior displayed by one member of a species toward an immature member of the same species (an immature conspecific) that increases the likelihood that the infant will survive (Numan & Insel, 2003). Depending on the species and its particular ecological niche, parental behavior can include maternal, paternal, and alloparental behavior, the latter being caretaking behaviors directed toward infants other than one’s own offspring. For mammals, the dominant care system relies on maternal behavior. In about 95% of mammalian species, the two sexes leave one another after mating, and once the pregnant female gives birth she cares for her offspring by herself (Numan & Young, 2015).

This uniparental maternal care system evolved because most lactating females can successfully raise young without the help of the male. About 5% of mammalian species, in contrast, exhibit a monogamous mating system where the male-female pair remains together following mating and both biological parents care for their offspring (maternal and paternal behavior). Examples include some rodent species, such as California mice and prairie voles, and certain species of New World monkeys, such as common marmosets and cotton-top tamarins (Kentner, Abizaid, & Bielajew, 2010).

While males do not lactate, they can directly care for infants in other ways, such as carrying them, huddling over them to keep them warm, or protecting them from threats. Monogamy occurs under ecological conditions where biparental care is necessary for infant survival (Brown, 1975). Alloparental behavior occurs in certain monogamous mammalian species when older siblings remain in the family group, instead of emigrating, and help their mother and father care for more recently born young. Such cooperatively breeding species include prairie voles, common marmosets, and early hominins (Hrdy, 2009; Numan, 2015).

In this essay, I will first describe the evolutionary conserved core neural circuits that regulate maternal behavior in nonhuman mammals. For the remainder of this paper, whenever I use the term animals, I will be specifically referring to nonhuman mammals. Since maternal behavior is a characteristic of all mammals, it is not surprising that a common neural network regulates the behavior across species (Numan & Insel, 2003). Panksepp (2011) has referred to this network as the Maternal Care System. Then I will describe the functional magnetic resonance imaging (fMRI) research that affirms for humans that similar neural regions are active when mothers view infant stimuli, presumably because they are imagining that they are engaging in caretaking activities.

This analysis will then be followed by a discussion of the possible neural basis of maternal love in humans. I use the term maternal love to refer to the pleasant and empathic feeling states that are associated with caring for one’s infant. Positive maternal feelings must interact with the core neural circuits of maternal behavior if feelings are to be translated into caregiving responses, and I will present neural models describing such an interaction. I am agnostic with respect to whether maternal love occurs in animals, since subjective feelings cannot be measured in animals, while humans can tell us about their subjective states.

My essay will conclude by comparing maternal behavior and love with paternal behavior and love, and with the long-term attachment and love that can occur between monogamous mating partners. It will be proposed that the neural circuits underpinning maternal behavior and maternal love may have provided a neural foundation for other types of caregiving behaviors and their associated emotional states (Numan, 2015; Numan & Young, 2015).

Descriptions of Maternal Behavior in Animals

The types of maternal behaviors shown by different mammalian mothers are influenced by the maturity of the young at birth (Numan & Insel, 2003). Infants can be born immature (altricial) and immobile, precocial and mobile, or intermediate between these two extremes. Rats, sheep, and rhesus monkeys are representative of each class, respectively. Rats give birth to their immobile pups in a secluded site where a nest is built, and where the mother nurses and licks (grooms) her young. She also retrieves displaced pups back to the nest site by carrying them in her mouth. Sheep give birth to relatively mature young that are mobile at birth. The mother nurses and grooms the young, but transport or retrieval behaviors do not occur, since the lamb can follow the mother.

In rhesus monkeys, initially the mother is in constant contact with her infant, nursing and grooming it, and the infant clings to its mother for transport. As the rhesus infant develops and becomes more mobile it wanders away from its mother, but the mother is usually aware of the infant’s location and if the infant is in danger the mother will move toward the infant and carry it away.

In all species, mothers are strongly attracted and attached to their infants until weaning. However, this mother-infant bond can be either nonselective or selective (Numan & Young, 2015), and this is dependent upon whether mixing and the potential confusion between one’s own young and those from another mother could occur under natural conditions. For example, rats form nonselective bonds with their young because in nature altricial young cannot move from one nest to another and therefore confusion between the infants of different mothers does not occur. As evidence, experimental cross-fostering tests show that postpartum rats will care for young that are not their own.

In contrast, sheep (and most primates) exhibit a selective bonding system. In sheep, lambs are born into a large herd and can move from one mother to another. Therefore, at the time of birth maternal sheep quickly learn the olfactory characteristics of their offspring and will subsequently care only for their own lamb, while rejecting the advances of alien young. Of course, under natural conditions, maternal rats learn the location of their nest site, which ensures that they are only taking care of their own young. But the point I am making here is that for the mechanisms underlying social bonding, maternal rats are attracted to a generic pup stimulus, while maternal sheep are ultimately attracted to a specific lamb stimulus.

In my discussion of the brain regions involved in maternal behavior in animals, the focus will be on those regions controlling maternal motivation or a mother’s interest in, and attraction toward, her young, rather than on brain regions which regulate specific maternal responses. Therefore, while rats retrieve their infants and sheep do not, damage to certain core neural regions disrupts maternal motivation in both species, so that they lose interest in their young, are no longer attracted to them, and therefore do not show their respective maternal responses (Numan, 2015).

Hormonal and Oxytocin Regulation of the Onset of Maternal Behavior in Animals

In most mammals, virgin (nulliparous = never having given birth) females avoid or reject infants, while parturient females show appropriate maternal behavior toward any conspecific infant at birth. In those species that develop selective attachments, this occurs as the mother interacts with her young during the early postpartum period and learns their particular stimulus characteristics.

What causes this change in the processing of infant stimuli by the brain, shifting such stimuli away from antisocial avoidance and rejection neural circuits in virgins and toward prosocial attraction and acceptance neural circuits in parturient females? In most mammals, hormonal and other physiological events at the end of pregnancy act on the brain to cause this change. The critical events include the hormones estradiol (an ovarian hormone) and prolactin (an anterior pituitary hormone), and the neuropeptide oxytocin. Estradiol and prolactin enter the brain from the peripheral blood supply, while oxytocin is produced in the hypothalamus, primarily from neurons in the paraventricular nucleus, which release oxytocin into diverse brain sites near the time of birth (Numan, 2015; Numan & Stolzenberg, 2009). [Oxytocin is also released into the peripheral blood supply by paraventricular nucleus axon terminals that project to the posterior pituitary, and in the periphery oxytocin stimulates uterine contractions and milk ejection from the mother’s nipples in response to suckling. However, unlike estradiol and prolactin, peripheral oxytocin has weak penetrance across the blood brain barrier. Therefore, it is the central release of oxytocin into the brain, where is serves as a neurotransmitter, that is important for maternal behavior.]

While estradiol, prolactin and oxytocin are essential for the onset of maternal behavior at parturition, they are not required for its maintenance during the remainder of the postpartum period. After a sufficient amount of postpartum maternal experience, it is likely that synapses become strengthened within certain key nodes of the maternal neural circuit so that maternal behavior can continue without hormonal and oxytocin stimulation (Numan, 2015; Numan & Young, 2015). Therefore, experience with infants coupled with the physiological events associated with late pregnancy and parturition cause neural changes that promote an enduring mother-infant bond. Which particular neural changes occur will be discussed in the section on brain circuits of maternal motivation.

Although oxytocin is not essential for the maintenance of maternal behavior, it does boost maternal motivation during the postpartum period (Numan, 2015). Oxytocin action on the brain causes increased licking and grooming of pups in postpartum rats, and is associated with increased levels of affectionate touching of infants by human mothers.

Finally, in those species that show paternal and/or alloparental behavior, it should be clear that mechanisms other than those related to pregnancy and parturition are involved in triggering these behaviors. Evolutionary processes are crucial: If paternal and/or alloparental behavior are necessary for infant survival, natural selection will create alternate mechanisms through which the parental circuitry can be activated. I will have more to say about these issues in subsequent sections.

Brain Circuits Regulating Maternal Motivation in Animals

A large body of experimental evidence has outlined the subcortical neural circuits regulating maternal motivation, and the medial preoptic area (MPOA), located in the hypothalamus, has been shown to play an essential role in all female mammals that have been examined (Dulac, O’Connell, & Wu, 2014; Lonstein et al., 2015; McHenry, Rubinow, & Stuber, 2015; Numan, 2015; Numan, 2007; Numan & Stolzenberg, 2009; Numan & Young, 2015). Destruction of MPOA neurons impairs the onset and maintenance of the behavior, and estradiol, prolactin and oxytocin act on MPOA to trigger the onset of maternal behavior.

 

A neural model of maternal behavior in animals. Nulliparous females typically avoid infant stimuli because they activate negatively valent amygdala (Amyg) neurons. Maternal behavior occurs because these avoidance responses are inhibited, while attraction toward infants is stimulated. Physiological events at the end of pregnancy cause the medial preoptic area (MPOA) to be activated by infant stimuli. MPOA projections then inhibit antisocial avoidance circuits and activate the mesolimbic dopamine (DA) reward system. The brain’s oxytocin (OT) system is also involved, with actions at several sites. In the amygdala, oxytocin stimulates positively valent neurons, while inhibiting negatively valent neurons. When oxytocin co-acts with dopamine in the nucleus accumbens (NA), it potentiates the inhibitory effects of dopamine, which releases the ventral pallidum from nucleus accumbens inhibition. This process allows the ventral pallidum (VP) to become responsive to infant stimuli arriving from positively valent amygdala neurons. The output of the ventral pallidum promotes maternal motivation. These events may also strengthen synapses between the amygdala and ventral pallidum (shown by a dashed circle), causing an enduring attraction between a mother and her infants. Neuronal, hormonal, and oxytocin effects ending in an arrow denote stimulation. Effects ending in a bar indicate inhibition. See text and Numan (2015) for more information. E = estradiol; Prl = prolactin; VTA = ventral tegmental area.

Figure 1: A neural model of maternal behavior in animals. Nulliparous females typically avoid infant stimuli because they activate negatively valent amygdala (Amyg) neurons. Maternal behavior occurs because these avoidance responses are inhibited, while attraction toward infants is stimulated. Physiological events at the end of pregnancy cause the medial preoptic area (MPOA) to be activated by infant stimuli. MPOA projections then inhibit antisocial avoidance circuits and activate the mesolimbic dopamine (DA) reward system. The brain’s oxytocin (OT) system is also involved, with actions at several sites. In the amygdala, oxytocin stimulates positively valent neurons, while inhibiting negatively valent neurons. When oxytocin co-acts with dopamine in the nucleus accumbens (NA), it potentiates the inhibitory effects of dopamine, which releases the ventral pallidum from nucleus accumbens inhibition. This process allows the ventral pallidum (VP) to become responsive to infant stimuli arriving from positively valent amygdala neurons. The output of the ventral pallidum promotes maternal motivation. These events may also strengthen synapses between the amygdala and ventral pallidum (shown by a dashed circle), causing an enduring attraction between a mother and her infants. Neuronal, hormonal, and oxytocin effects ending in an arrow denote stimulation. Effects ending in a bar indicate inhibition. See text and Numan (2015) for more information. E = estradiol; Prl = prolactin; VTA = ventral tegmental area.

 

Fig. 1 presents a theoretical neural model, built upon evidence (Numan, 2015; Numan, 2007), which depicts the larger neural circuitry within which the MPOA operates. Before describing the details, a simple way to understand this figure is to say that MPOA outputs have two important functions: They activate the brain’s reward system so that infant stimuli become attractive and rewarding and they inhibit aversion or antisocial neural networks so that infant stimuli lose the ability to activate avoidance and rejection responses.

MPOA neural connections to the mesolimbic dopamine system are crucial for the rewarding aspects of maternal motivation (Numan, 2015; Numan & Stolzenberg, 2009). The mesolimbic dopamine system, an important component of the brain’s reward system, includes dopamine neurons in the ventral tegmental area of the midbrain that project upstream to the nucleus accumbens in the forebrain. Note that nucleus accumbens projection neurons inhibit the nearby ventral pallidum. The model in Fig. 1 proposes that hormones prepare the MPOA to be responsive to infant stimuli. Infant stimuli then activate MPOA projections to the ventral tegmental area, which stimulate dopamine release into the nucleus accumbens. Dopamine acts to inhibit the nucleus accumbens, in this way releasing the ventral pallidum from inhibition. Such a mechanism allows the ventral pallidum to become responsive to infant stimuli that reach the ventral pallidum via the amygdala.

The resultant stimulated output of ventral pallidum attraction/reward circuits gives rise to motivated responses that attract a mother to her young. Therefore, it is the output of ventral pallidum, triggered by MPOA activity, which is critical for maternal motivation (Numan & Stolzenberg, 2009). If one were to prevent ‘maternal’ MPOA neurons from interacting with dopamine neurons in the ventral tegmental area, then the mother would lose interest in her young, would no longer be attracted to them, and would not care for them (Numan & Stolzenberg, 2009). The MPOA also projects to the oxytocin neurons in the paraventricular nucleus, stimulating the release of oxytocin into diverse sites that include MPOA, ventral tegmental area, nucleus accumbens, and amygdala. Oxytocin, therefore, acts to promote neural activity across the circuit that allows the MPOA to trigger ventral pallidum output in response to infants, in this way contributing to the onset of maternal behavior at parturition.

The amygdala, a critical site in the model (Numan, 2007; Numan, 2015; Numan et al., 2010), is functionally heterogeneous, and different neurons respond to either pleasant or aversive stimuli (positively valent or negatively valent neurons). When infant stimuli are processed through negatively valent amygdala neurons that project to antisocial circuits, the avoidance and rejection responses typically shown by virgins occur. As shown in Fig. 1, when the MPOA is appropriately primed at the end of pregnancy, it not only stimulates prosocial reward circuits (mesolimbic dopamine system), but it also inhibits the antisocial circuits. Further, oxytocin action on the amygdala potentiates the responsiveness of positively valent neurons to infant stimuli while inhibiting negatively valent neurons (Numan, 2007; Numan, 2015).

Why are estradiol, prolactin, and oxytocin essential for the onset, but not the maintenance, of maternal behavior? A strong possibility is that during an initial maternal experience with infants at parturition, the hormone primed MPOA stimulates dopamine and oxytocin release into the nucleus accumbens. Dopamine and oxytocin co-act to strongly inhibit the nucleus accumbens, which, in turn, activates mechanisms that strengthen the synapses between positively valent amygdala neurons and ventral pallidum (see Fig. 1), causing the development of an enduring attraction between a mother and her infants (Numan & Young, 2015). This process would be akin to the development of long-term potentiation (LTP) between the amygdala-to-ventral pallidum connections. These neural plasticity effects are important because although the physiological events of late pregnancy synchronize the onset of maternal behavior with the birth of the young, in order for the young to survive, maternal behavior must continue after the events which triggered its onset have waned. As I will describe at the end of this paper, similar neural and neurochemical mechanisms may underlie the formation of other types of enduring social bonds in animals and humans.

The Neurobiology of Maternal Behavior and Maternal Love in Humans

Although for most mammals the physiological events of late pregnancy stimulate the onset of maternal behavior, such events are not required in some species: allomaternal behavior, where adult virgin females care for conspecific young, occurs in certain species (Numan & Insel, 2003), and evidence shows that MPOA activity along with dopamine and oxytocin action on the nucleus accumbens are involved (Numan, 2015; Numan & Young, 2015; Tsuneoka et al., 2013). In these species, infant stimuli, in the absence of parturition-associated events, have easy access to MPOA neural circuits, triggering parental motivation.

Hrdy (2009) has proposed that allomaternal behavior was crucial for infant survival during early human evolution, and this may explain why human maternal motivation is relatively emancipated from hormones, which would allow for the adoption of infants by nulliparous women. However, maternal motivation is not all-or-none, and research shows that the endocrine events of parturition do boost maternal motivation in women (Numan & Insel, 2003; Saltzman & Maestripieri, 2011). Even with such hormonal stimulation, experiential factors also seem to be important for the development of optimal maternal behavior: in monkeys and apes, the mortality rate of infants born to first-time mothers [primiparous females] is much higher than that for mothers who have previously given birth [multiparous females] (Hrdy, 1999). These data lead to the possibility that for those nulliparous women who adopt infants, experiential factors associated with mothering, in the absence of hormones, may enhance maternal motivation over time. Experimental evidence shows that such a process does indeed occur in rodent species that exhibit allomothering (Numan & Insel, 2003; Stolzenberg & Rissman, 2011). Although allomaternal rodents will initially care for young in their home cages, they will not retrieve young in a novel environment. With maternal experience, such retrieval responses do occur.

Brain Circuits and Maternal Motivation in Women

Recent reviews on the neurobiology of maternal behavior in women (Feldman, 2015; Lonstein et al., 2015; Numan, 2015; Rilling, 2013; Rilling & Young, 2014; Strathearn, 2011; Swain, 2011) have shown that when postpartum mothers are exposed to infant stimuli (usually infant faces or infant cries) while in an fMRI scanner, blood oxygen level dependent (BOLD) signals (a proxy for neural activity) increase in the hypothalamus, ventral tegmental area, ventral pallidum, and amygdala, and such increases have been correlated with increases in peripheral blood levels of oxytocin (peripheral oxytocin release from paraventicular nucleus axon terminals in the posterior pituitary is presumed to reflect its central release into brain sites such as MPOA, nucleus accumbens, and amygdala).

These results conform to the animal research, where infants activate MPOA stimulation of the mesolimbic dopamine and oxytocin systems, so that amygdala input to ventral pallidum can be processed to promote caregiving responses. Because of the small size of the hypothalamus, and the low spatial resolution of fMRI, it is difficult to distinguish between different hypothalamic nuclei, such as the MPOA and paraventricular nucleus, but as fMRI technology advances, such distinctions are likely to be made. Since the animal research stresses the importance of MPOA neurons for maternal behavior, it would be important to verify that this core neural region is also important in humans, which would emphasize the evolutionarily conserved nature of the essential maternal circuitry. Also, different neuronal groups undoubtedly play different roles in human maternal responsiveness. By distinguishing MPOA activity from that of the paraventricular nucleus, one might gain insights into the particular functions of each area.

Although nulliparous women may be attracted to infants (Glocker et al., 2009), this is not the same as devoting one’s life to the care of an infant. As indicated above, the physiological events associated with the end of pregnancy coupled with postpartum maternal experience, or the maternal experience associated with extensive mother-infant interactions in those nulliparous women who choose to adopt, appear to modify brain circuits to boost maternal motivation. There is support for this proposal. Recall that animal research shows that for postpartum females infant stimuli activate amygdala prosocial circuits, while for most nulliparous females, such stimuli activate amygdala aversion circuits. Relevantly, in postpartum women, amygdala BOLD signals increase when a mother views pictures of her infant (Barrett et al., 2011). With respect to infant cries, such stimuli could promote approach and caregiving responses in mothers, but they might also promote annoyance and avoidance, particularly in nonmothers.

For postpartum women, Kim et al. (2011) reported that own baby cries caused BOLD activations in several brain regions, including the amygdala and ventral pallidum, and that such activations were particularly prominent in women who were breast feeding their infant (suckling stimulation activates the oxytocin system). Behavioral measures of maternal behavior (taken outside the scanner at 3-4 months postpartum) also indicated that better maternal behavior (affectionate touch; vocal clarity; mother-infant eye contact; supportive presence; consistency of style) was associated with greater own baby cry-induced activity in amygdala and ventral pallidum.

One interpretation of these findings is that oxytocin, along with other factors, such as MPOA activation of dopamine release into the nucleus accumbens, promoted amygdala activation of the ventral pallidum, which would lead to either imagined (in the scanner) or overt (outside the scanner) proactive aid-giving responses to infant distress signals. In contrast to these findings in postpartum women, Reim et al. (2011) found that while infant cries activated the amygdala in nulliparous women, intranasal oxytocin administration, which would increase oxytocin brain levels, decreased this amygdala response. Careful studies using advanced imaging techniques will be needed to determine whether the amygdala areas activated by infant cries are the same or different in nulliparous and postpartum women. One possibility is that for nulliparous females, infant cries primarily activate negatively valent amygdala neurons that project to avoidance circuits, with the response of these neurons being reduced by oxytocin, while in postpartum women infant cries activate positively valent amygdala neurons that project to ventral pallidum attraction circuits, with this response being potentiated by endogenous oxytocin.

The importance of this analysis for maternal pathologies in human mothers, such as the occurrence of child abuse and neglect, should be considered (McHenry et al., 2015; Numan & Insel, 2003). If periparturitional physiological events and/or extensive maternal experience downregulate avoidance systems and upregulate attraction systems in women, then if something were to go wrong with such mechanisms, maternal behavior could become abnormal. In support, women with postpartum depression exhibit poor maternal behavior and these mothers also show reduced BOLD responses within the mesolimbic dopamine system in response to hearing their own infant crying (Laurent & Ablow, 2012).

My analysis is also important for an understanding of the intergenerational continuity of abnormal maternal behavior in humans. Children who have been physically, emotionally, or sexually abused, or neglected by their parents, tend to become abusive or neglectful parents when they have their own offspring (Numan & Insel, 2003). For example, approximately 30% of abused children become abusive parents. These human studies, of course, do not resolve whether the intergenerational continuity of abnormal maternal behavior is due to genetic inheritance, the early adverse effects of poor parenting on the child’s development, or both. However, experimental studies on rhesus monkeys emphasize the important role of the early adverse effects of poor parenting on the subsequent parental behavior of the affected offspring. Female rhesus infants that are born to known abusive mothers and are cross-fostered to normal mothers near the time of birth grow up to show normal maternal behavior, while approximately 50% of infant females that are born to normal mothers and are cross-fostered to abusive mothers grow up to show abusive responses to their own offspring (Maestripieri, 2005). Such abuse is characterized by bouts of hitting, biting, throwing, crushing, and rejecting the infant.

Multiple mechanisms are likely to be involved in how exposure to abuse and/or neglect causes an infant to develop faulty maternal behavior in adulthood (Numan, 2015). One possibility is that being abused or neglected by one’s parent results in a dysfunctional development of maternal neural circuits in the female offspring, leading to abnormal maternal behavior once the affected offspring have their own children (Champagne, 2008; Numan, 2015; Numan & Stolzenberg, 2009). Animal evidence supports such a view. Rhesus monkeys reared without their mother (a model of maternal neglect) have lower levels of oxytocin in their cerebrospinal fluid than do mother-reared monkeys (Winslow et al., 2003). Importantly, rhesus females raised without their mothers tend to abuse or neglect their own offspring in adulthood (Numan & Insel, 2003).

For rats, infants that receive low levels of licking/grooming from their mothers develop lower levels of estradiol receptors and oxytocin receptors in their MPOA when compared to their counterparts that receive higher levels of licking/grooming (Champagne, 2008). Therefore, the MPOA of rats exposed to low levels of licking/grooming as infants would be less responsive to estradiol and oxytocin in adulthood, and this would presumably result in a lower level of MPOA activation of the mesolimbic dopamine system (Numan & Stolzenberg, 2009; Stolzenberg & Champagne, 2015). Significantly, such rats grow up to show low levels of licking and grooming toward their own offspring. Cross-fostering experiments show that these effects are due to early experience and not genetic inheritance.

Brain Circuits and Maternal Love in Women

While subcortical mechanisms (such as those involving the hypothalamus and its connections to the mesolimbic dopamine system) are critically involved in behavioral control (Numan & Woodside, 2010), research has concentrated on cortical mechanisms when investigating feeling states in humans. Human neuroimaging studies have correlated activity within the orbitofrontal cortex and its connections to the insular cortex with a variety of subjective feeling states, including positive emotions and empathy (Berridge & Kringelbach, 2015; Craig, 2009; Engen & Singer, 2013).

Amygdala projections to the orbitofrontal and insular regions may be one route over which various emotions are subjectively experienced (Barbas et al., 2011). Positive feeling states and empathy may trigger approach behaviors and caregiving responses by interacting with subcortical motivational systems: the orbitofrontal and insular cortex project to the medial prefrontal cortex, which, in turn, projects to the hypothalamus (Nieuwenhuys, 2012; Price, 2005). Therefore, an orbitofrontal/insular cortex-to-medial prefrontal cortex-to-hypothalamus circuit could be a route over which subjective feeling states are translated into caregiving behaviors.

Although a rudimentary circuit similar to the one just described may exist in animals, in my opinion, the driving of caregiving behaviors by positive and empathic feeling states most likely fully evolved in human societies, where high levels of cooperation and mutual aid-giving are essential for survival (Numan, 2015). In fact, because the maternal care system is the most elemental aid-giving system, empathic driving of aid-giving behaviors may have first evolved within the context of human mother-infant relationships, with aspects of this neural system subsequently serving as the foundation for other types of strong cooperative social bonds in humans (Hrdy, 2009; Brown, Brown, & Penner, 2012; Numan, 2015; Numan & Young, 2015; see last section of this essay).

With respect to the human maternal care system, I have proposed that infant stimuli reach the orbitofrontal/insular cortex via the amygdala to give rise to feeling states that we could refer to as maternal love, and subsequent inputs to the MPOA via the medial prefrontal cortex may influence overt caregiving responses toward infants (Numan, 2015). This foundational neural circuitry connecting maternal emotion (love) with maternal motivation (attraction toward, and acceptance of, infants) is depicted in Fig. 2.

Figure 2: A neural model depicting how feelings of maternal love are translated into overt caregiving responses in human mothers. The maternal behavior part of the model, involving medial preoptic area (MPOA) activation of the mesolimbic dopamine (DA) system, is derived from Figure 1. In the model, positively valent amygdala (Amyg) neurons that are responsive to infant stimuli not only project to the ventral pallidum (VP: part of the behavioral circuit), but also project to the orbitofrontal cortex and insular cortex (OF/IC), and activity at these latter sites is proposed to give rise to feelings of maternal love. In order for such feelings to be translated into caregiving behaviors, the orbitofrontal/insular cortex projects to the medial prefrontal cortex (MPFC), which then activates the MPOA and maternal behavior. Oxytocin (OT) acts on the amygdala to stimulate the output of positively valent neurons, and it undoubtedly acts at other sites as well (see Fig. 1). Neurons ending in an arrow are excitatory, and those ending in a bar are inhibitory. See the text and Numan (2015) for a more information. NA = nucleus accumbens; VTA = ventral tegmental area.

Figure 2: A neural model depicting how feelings of maternal love are translated into overt caregiving responses in human mothers. The maternal behavior part of the model, involving medial preoptic area (MPOA) activation of the mesolimbic dopamine (DA) system, is derived from Figure 1. In the model, positively valent amygdala (Amyg) neurons that are responsive to infant stimuli not only project to the ventral pallidum (VP: part of the behavioral circuit), but also project to the orbitofrontal cortex and insular cortex (OF/IC), and activity at these latter sites is proposed to give rise to feelings of maternal love. In order for such feelings to be translated into caregiving behaviors, the orbitofrontal/insular cortex projects to the medial prefrontal cortex (MPFC), which then activates the MPOA and maternal behavior. Oxytocin (OT) acts on the amygdala to stimulate the output of positively valent neurons, and it undoubtedly acts at other sites as well (see Fig. 1). Neurons ending in an arrow are excitatory, and those ending in a bar are inhibitory. See the text and Numan (2015) for a more information. NA = nucleus accumbens; VTA = ventral tegmental area.

 

Human neuroimaging studies have clearly shown that the orbitofrontal/insular cortex is activated when mothers are exposed to stimuli from their infants (Minagawa-Kawai et al., 2009; Nitschke et al., 2004; Parsons et al., 2013; Rocchetti et al., 2014), with such BOLD responses being positively correlated with the mothers’ reported pleasant mood ratings (Nitschke et al., 2004). Additionally, intranasal oxytocin administration further enhances these BOLD responses (Rocchetti et al., 2014), perhaps because oxytocin potentiates amygdala projections to the orbitofrontal/insular regions.

Finally, when mothers are exposed to their infant’s cries, activity within the orbitofrontal/insular regions is associated with increased BOLD responses within the hypothalamus, amygdala, and ventral pallidum (Hipwell et al., 2015). The basic circuit outlined in Fig. 2 is a working hypothetical model. Further, it should be obvious that the full appreciation of the maternal state would be the result of the interaction of this basic circuit with neocortical brain systems controlling higher order cognitive and perceptual processes (Feldman, 2015).

The goal of my analysis has been to show that by integrating animal and human research, one begins to understand the neural circuits and neurochemicals through which maternal love can influence maternal behavior. Dysfunctions within either the motivational or emotional circuitry could have profound effects, leading to abnormal maternal behavior and to the development of pathological feeling states and social behaviors in the infants raised by such mothers (Numan, 2015; Numan & Insel, 2003). Further, by understanding this circuitry, biological (pharmacological) therapies, such as oxytocin administration, might ameliorate certain pathologies of maternal responsiveness.

Paternal Behavior and Paternal Love

In the 5% of mammalian species that are monogamous, the father may directly care for the young. The available animal research shows that when paternal behavior occurs, its neural network matches that for maternal behavior (Dulac et al., 2014; Numan, 2015; Tachikawa et al., 2013; Wu et al., 2014): MPOA, nucleus accumbens, ventral pallidum, amygdala, and oxytocin systems are all involved. Since males are not exposed to the hormones of pregnancy, other factors must activate the parental network that males share with females, and these factors include mating and cohabitating with a pregnant female.

The question of paternal behavior and paternal love in men, and whether a paternal neural network matches a women’s maternal network is a difficult one. Although many human societies are monogamous (or at least serially monogamous), paternal behavior, involving direct and extensive care of infants, in human societies has historically been considered facultative, that is optional and situation-dependent (Hrdy, 2009). In several human societies, the mother is the primary caregiver, while fathers play a secondary role (see Hrdy 2009 for a detailed analysis). It is possible, however, that when fathers do assume a primary caretaking role, direct father-child interactions ultimately engage many components of the same neural network that regulates maternal behavior and maternal love in women, and such a proposal fits with the animal research on paternal behavior.

As an example, in a neuroimaging study, Abraham et al. (2014) have reported that primary caregiving mothers and fathers show greater amygdala activation in response to infant stimuli than do fathers who assumed a secondary caregiver role. Primary caregivers were defined as those parents who spent the most time directly caring for and interacting with the infant, and in interviews, individuals clearly defined themselves as either a primary or secondary caregiver. In other studies, intranasal oxytocin administration was found to improve father-child interactions during a play session (Naber et al., 2010; Weisman et al., 2012). On the assumption that most of the fathers in these two latter studies were likely to be secondary caregivers, perhaps when fathers assume a primary role in childcare, experience-induced increases in endogenous oxytocin improve their parenting. These results suggest that, as for nulliparous women who adopt infants, extensive father-infant interactions may boost paternal motivation. Perhaps MPOA-induced release of oxytocin into brain sites such as the amygdala and nucleus accumbens are involved. For more information about the human paternal brain, see Feldman (2015).

Monogamy and Long-Term Attachment and Love Between Mating Partners

Most mammals are polygamous and mating partners do not form a pair bond. Once sexual activity concludes, the two sexes leave one another and the female rears the young by herself. Therefore, the most common enduring mammalian social bond is the mother-infant bond, which lasts, at least, until the young are weaned. In the 5% of mammalian species that exhibit a monogamous mating system, the partners remain together once mating is consummated, and an enduring bond is formed between mating partners. Because the mother-infant bond occurs in all mammals, while the monogamous pair bond is rare, it has been proposed that the mother-infant bonding mechanism provided the neural foundation for the pair bond (Numan, 2015; Numan & Young, 2015).

Numan and Young (2015) compared the details of the neural mechanisms that underlie the mother-infant bond in animals with the pair bond that forms after mating in monogamous prairie voles. Remarkable similarities were detected, with the amygdala, nucleus accumbens, and ventral pallidum being involved. Evidence also suggests that high levels of oxytocin action within the nucleus accumbens, combined with dopamine release at this site, co-act to promote the synaptic plasticity that allows either infant stimuli or mating partner stimuli derived from the amygdala to persistently activate the ventral pallidum, leading to an enduring social attraction either towards one’s infant or mate.

Some of these mechanisms might also contribute to the long-term attachment (and love) that occurs in many human couples (Numan, 2015). Schneiderman et al. (2012) measured blood levels of oxytocin in new lovers 3 months after the initiation of a romantic relationship, and such oxytocin levels were higher than those measured in non-attached single individuals. More importantly, oxytocin levels varied in the new lovers, and those couples that had higher levels of oxytocin at 3 months were more likely to have stayed together in their relationship 6 months later. Further, in an fMRI study, Acevedo et al. (2012) measured the BOLD response in various brain regions when individuals viewed facial images of their partners, or control faces. Some of the subjects were in the early stages of a romantic relationship, while others were in a long-term relationship.

The ventral tegmental area was activated to a greater extent when all couples viewed images of their partner, but the ventral pallidum was more highly active only when subjects in long-term relationships viewed images of their partner. The authors note that this same brain region (ventral pallidum) is active when mothers view images of their own infants. These results fit with the idea that the strengthening of connections between the amygdala and the ventral pallidum, assumed to be due to the inhibitory actions of oxytocin and dopamine on the nucleus accumbens, may contribute to both the mother-infant bond and the monogamous bond. These results also support the view that the maternal bonding system may have provided the basic neural foundation for other types of strong social bonds.

Why do certain spouses remain together for life, while other human couples have more tenuous bonds? Multiple factors undoubtedly influence long-term attachments and love, but genetic and experiential factors are sure to be involved (Numan, 2015; Young & Alexander, 2012). For example, there are different variants of the oxytocin receptor gene (different alleles), and some variants may give rise to oxytocin receptors that poorly bind oxytocin. In addition, as mentioned previously, poor parenting can disrupt the development of neural systems that control parental behavior in the affected offspring. To the extent that the parental circuitry serves as a foundation for other bonding systems, this could lead to the development of weak bonds between an affected individual and his/her partner in adulthood, in addition to poor parental behavior.

References

Abraham, E., Hendler, T., Shapira-Lichter, I., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2014). Father’s brain is sensitive to childcare experiences. Proceedings of the National Academy of Sciences USA, 111, 9792-9797.

 

Acevedo, B.P., Aron, A., Fisher, H.E., & Brown, L.L. (2012). Neural correlates of long-term intense romantic love. Social, Cognitive, and Affective Neuroscience, 7, 145-159.

 

Barbas, H., Zikopoulos, B., & Timbie, C. (2011). Sensory pathways and emotional context for action in primate prefrontal cortex. Biological Psychiatry, 69, 1133-1139.

 

Barrett, J., Wonch, K.E., Gonzalez, A., Ali, N., Steiner, M., Hall, G.B., & Fleming, A.S. (2012). Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Social Neuroscience, 7, 252-268.

 

Berridge, K.C., & Kringelbach, M.L. (2015). Pleasure systems in the brain. Neuron, 86, 646-664.

 

Brown, J.L. (1975). The evolution of behavior. New York: Norton.

 

Brown, S.L., Brown, R.M., & Penner, L.A. (2012). Moving beyond self-interest: Perspectives from evolutionary biology, neuroscience, and the social sciences. New York: Oxford.

 

Champagne, F.A. (2008). Epigenetic mechanisms and the transgenerational effects of maternal care. Frontiers in Neuroendocrinology, 29, 386-397.

 

Craig, A.D. (2009). How do you feel now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59-70.

 

Dulac, C., O’Connell, L.A., & Wu, Z. (2014). Neural control of maternal and paternal behaviors. Science, 345, 765-770.

 

Engen, H.G., & Singer, T. (2013). Empathy circuits. Current Opinion in Neurobiology, 23, 275-283.

 

Feldman, R. (2015). The adaptive human parental brain: implications for children’s social development. Trends in Neurosciences, 38, 387-399.

 

Glocker, M.L., Langleben, D.D, Ruparel, K., Loughead, J.W., Valdez, J.N., Griffin, M.D., …Gur, R.C. (2009). Baby schema modulates the brain reward system in nulliparous women. Proceedings of the National Academy of Sciences USA, 106, 9115-9119.

 

Hipwell, A.E., Guo, C., Phillips, M.L., Swain, J.E., & Moses-Kolko, E.L. (2015). Right frontoinsular cortex and subcortical activity to infant cry is associated with maternal mental state talk. Journal of Neuroscience, 35, 12725-12732.

 

Hrdy, S.B. (1999). Mother nature. New York: Pantheon.

 

Hrdy, S.B. (2009). Mothers and others. Cambridge: Belknap.

 

Kim, P., Feldman, R., Mayes, L.C., Eicher, V., Thompson, N., Leckman, J.F., & Swain, J.E. (2011). Breastfeeding, brain activation to own infant cry, and maternal sensitivity. Journal of Child Psychology and Psychiatry, 52, 907-915.

 

Kentner, A.C., Abizaid, A., & Bielajew, C. (2010). Modeling dad: Animal models of paternal behavior. Neuroscience and Biobehavioral Reviews, 34, 438-451.

 

Laurent, H.K., & Ablow, J.C. (2012). A cry in the dark: depressed mothers show reduced neural activation to their own infant’s cry. Social, Cognitive, and Affective Neuroscience, 7, 125-134.

 

Lonstein, J.S., Levy, F., Fleming, A.S. (2015). Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals. Hormones and Behavior, 73, 156-185.

 

Maestripieri, D. (2005). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences USA, 102, 9726-9729.

 

McHenry, J.A., Rubinow, D.R., & Stuber, G.D. (2015). Maternally responsive neurons in the bed nucleus of the stria terminalis and medial preoptic area: Putative circuits for regulating anxiety and reward. Frontiers in Neuroendocrinology, 38, 65-72.

 

Minagawa-Kawai, Y., Matsuoka, S., Dan, I., Naoi, N., Nakamura, K., & Kojima, S. (2009). Prefrontal activation associated with social attachment: Facial-emotion recognition in mothers and infants. Cerebral Cortex, 19, 284-292.

 

Naber, F., van IJzendoorn, M.H., Deschamps, P., van Engeland, H., & Bakermans-Kranenburg, M.J. (2011). Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: A double-blind within-subject experiment. Psychoneuroendocrinology, 35, 1583-1586.

 

Nieuwenhuys, R. (2012). The insular cortex: a review. Progress in Brain Research, 195, 123-163.

 

Nitschke, J.B., Nelson, E.E., Rusch, B.D., Fox, A.S., Oakes, T.R., & Davidson, R.J. (2004). Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. NeuroImage, 21, 583-592.

 

Numan, M. (2007). Motivational systems and the neural circuitry of maternal behavior in the rat. Developmental Psychobiology, 49, 12-21.

 

Numan, M. (2015). Neurobiology of social behavior: Toward an understanding of the prosocial and antisocial brain. Amsterdam: Elsevier.

 

Numan, M., Bress, J.A., Ranker, L.R., Gary, A.J., Denicola, A.L., Bettis, J.K., & Knapp, S.E. (2010). The importance of the basolateral/basomedial amygdala for goal-directed maternal responses in postpartum rats. Behavioural Brain Research, 214, 368-376.

 

Numan, M., & Insel, T.R. (2003). The neurobiology of parental behavior. New York: Springer.

 

Numan, M., & Stolzenberg, D.S. (2009). Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Frontiers in Neuroendocrinology, 30, 46-64.

 

Numan, M., & Woodside, B. (2010). Maternity: Neural mechanisms, motivational processes, and physiological adaptations. Behavioral Neuroscience, 124, 715-741.

 

Numan, M., & Young, L.J. (2015). Neural mechanisms of mother-infant bonding and pair bonding: Similarities, differences, and broader implications. Hormones and Behavior, http://dx.doi.org/10.1016/j.yhbeh.2015.05.015.

 

Panksepp, J. (2011). The basic emotional circuits of mammalian brains: Do animals have affective lives. Neuroscience and Biobehavioral Reviews, 35, 1791-1804.

 

Parsons, C.E., Stark, E.A., Young, K.S., Stein, A., & Kringelbach, M.L. (2013). Understanding the human parental brain: a critical role of the orbitofrontal cortex. Social Neuroscience, 8, 525-543.

 

Price, J.L. (2005). Free will versus survival: brain systems that underlie intrinsic constraints on behavior. Journal of Comparative Neurology, 493, 132-139.

 

Riem, M.M.E., Bakersmans-Kranenburg, M.J., Pieper, S., Tops, M., Boksem, M.A.S., Vermeiren, R.R.J.M., …Rombouts, S.A.R.B. (2011). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biological Psychiatry, 70, 291-297.

 

Rilling, R.K. (2013). The neural and hormonal bases of human parental care. Neuropsychologia, 51, 731-747.

 

Rilling, R.K., & Young, L.J. (2014). The biology of mammalian parenting and its effects on offspring social development. Science, 345, 771-776.

 

Rocchetti, M., Radua, J., Paloyelis, Y., Xenaki, L.A., Frascarelli, M., Caverzasi, E., …Fusar-Poli, P. (2014). Neurofunctional maps of the ‘maternal brain’ and the effects of oxytocin: A multimodal voxel-based meta-analysis. Psychiatry and Clinical Neurosciences, 68, 733-751.

 

Saltzman, W., & Maestripieri, D. (2011). The neuroendocrinology of primate maternal behavior. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 35, 1192-1204.

 

Schneiderman, I., Zagoory-Sharon, O., Leckman, J.F., & Feldman, R. (2012). Oxytocin during the initial stages of romantic attachment: relations to couples’ interactive reciprocity. Psychoneuroendocrinology, 37, 1277-1285.

 

Stolzenberg, D.S., & Champagne, F.A. (2015). Hormonal and non-hormonal bases of maternal behavior: The role of experience and epigenetic mechanisms. Hormones and Behavior, http://dx.doi.org/10.1016/j.yhbeh.2015.07.005.

 

Stolzenberg, D.S., & Rissman, E.F. (2011). Oestrogen-independent, experience-induced maternal behavior in female mice. Journal of Neuroendocrinology, 23, 345-354.

 

Strathearn, L. (2011). Maternal neglect: oxytocin, dopamine, and the neurobiology of attachment. Journal of Neuroendocrinology, 23, 1054-1065.

 

Swain, J.E. (2011). The human parental brain: in vivo neuroimaging. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 35, 1242-1254.

 

Tachikawa, K.S., Yoshihara, Y., & Kuroda, K.O. (2013). Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. Journal of Neuroscience, 33, 5120-5126.

 

Tsuneoka, Y., Maruyama, T., Yoshida, S., Nishimori, K., Kato, T., Numan, M., & Kuroda, K.O. (2013). Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. Journal of Comparative Neurology, 521, 1633-1663.

 

Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2012). Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement. Biological Psychiatry, 72, 982-989.

 

Winslow, J.T., Noble, P.L., Lyons, C.K., Sterk, S.M., & Insel, T.R. (2003). Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology, 28, 910-918.

 

Wu, Z., Autry, A.E., Bergan, J.F., Watabe-Uchida, M., & Dulac, C.G. (2014). Galanin neurons in the medial preoptic area govern parental behaviour. Nature, 509, 325-330.

 

Young, L., & Alexander, B. (2012). The chemistry between us: love, sex, and the science of attraction. New York: Penguin.

 

 

 

 

 

 

 

Print Friendly, PDF & Email
Share

Traffic Count

  • 215966Total reads:
  • 116Reads today:
  • 171755Total visitors:
  • 92Visitors today: