The current study demonstrates associations between breastfeeding and maternal brain responses to own infant stimuli as well as dyadic parenting behaviors in the early postpartum period. During the first postpartum month, several limbic and cortical brain regions previously shown to be important for caregiving behaviors and empathy, were more active among breastfeeding mothers compared to formula-feeding mothers while listening to their own baby versus a control baby-cry. Furthermore, for all the mothers in the study (breastfeeding and formula-feeding), the degree of activation in these brain regions in responses to own baby-cry at the first postpartum month was correlated with greater maternal sensitivity observed during dyadic mother-infant interactions that were videotaped at 3-4 months postpartum. These findings relate the neural processing of infant sensory cues by mothers and the development of maternal responsiveness as infants begin to take an active part in dyadic interactions.
As predicted, we found differences between breastfeeding and formula-feeding mothers in activations in the amygdala, putamen, globus pallidus, and superior frontal gyrus in response to their own baby's cry. Rodent studies have consistently shown that activations in these brain regions and the connections between them are correlated with the emergence of maternal behavior (Mello & Villares, 1997
), and lesions in these circuits can severely impair the expression of maternal behavior (Numan, 2007
; Numan & Smith, 1984
). Similar findings have been reported in human studies when mothers were exposed to salient infant stimuli including baby cries, still photographs, or video clips (Noriuchi, Kikuchi, & Senoo, 2008
; Ranote et al., 2004
; Strathearn, Fonagy, Amico, & Montague, 2009
; Strathearn, Li, Fonagy, & Montague, 2008
; Swain et al., 2008
). The brain areas implicated included portions of the mirror-neuron circuits (inferior frontal gyrus, superior temporal gyrus, insula, and fusiform gyrus). These circuits are important for processing the emotional states of others (Iacoboni & Dapretto, 2006
; Völlm et al., 2005
). Lenzi et al. (2009)
found that parent responses to pictures of their own infant in these mirror-neuron circuits were related to parental reflective functioning. Thus, higher activations in these brain regions contribute to breastfeeding mother's ability to understand their own infant's emotional state and respond in an appropriate way to the infant's needs.
Breastfeeding mothers exhibited a trend toward higher maternal sensitivity during mother-infant interaction at 3-4 months postpartum as compared to formula-feeding mothers. The idea that the greater maternal brain activations among breastfeeding mothers may facilitate greater behavioral sensitivity to the infant is also supported by the finding of significant correlation between brain activations and maternal sensitivity in dyadic interactions observed 3 to 4 months postpartum. Importantly, sensitive maternal behavior observed in dyadic mother-child interactions at 3 months has been shown to be associated with improved cognitive, social, emotional, and moral development across childhood and up to adolescence (Feldman, 2007b
; Feldman, Greenbaum, & Yirmiya, 1999
; Isabella & Belsky, 1991
It is important to note that the relationship of breastfeeding with greater maternal brain responses and more sensitive maternal behaviors may not be causal and confounded by other factors. For example, one possible mechanism underlying the relationships between breastfeeding, greater activations in the maternal circuits, and the mother's later sensitivity to infant stimuli could be due to the effects of the neurohormones involved in nursing, such as oxytocin. Oxytocin, which is synthesized in the hypothalamus and released from the posterior pituitary, stimulates milk release at the mammary glands. Oxytocin also facilitates other maternal behaviors in animal studies (Febo, Numan, & Ferris, 2005
). Higher levels of peripheral oxytocin have been associated with sensitive and synchronous parental behaviors in human mothers and fathers (Feldman, Weller, Zagoory-Sharon, & Levine, 2007
). In human fMRI research, brain responses to own baby-cry at the first month postpartum were increased in mothers who delivered vaginally compared with cesarean section (Swain, et al., 2008
), which has been linked to decreased oxytocin (Kendrick, 2000
). Peripheral maternal oxytocin levels, in response to dyadic interactions at 7 months postpartum, was associated with hypothalamic activation in the mother's brain in response to viewing pictures of their infant at 11 months postpartum (Strathearn, Fonagy, et al., 2009
). The duration of breastfeeding may be related to the oxytocin levels and play a role in maternal sensitivity and infants' outcomes (Kramer, et al., 2008
). It is possible that differences in regional brain activation seen in this study are due to the act of breastfeeding and the increased release of oxytocin. In future studies, it will be important to include measures of oxytocin and other related neurohormones such as prolactin directly.
Another potentially confounding issue concerns the factors which influence a mother's decision to breastfeed before the child is born. For example, Britton and colleagues (2006)
found that intention to breastfeed prior to the child's birth predicted maternal sensitivity at three months postpartum. Likewise, mothers who experienced consistent and positive care in childhood are also more likely to provide warm and sensitive parenting to their children (Belsky, Jaffee, Sligo, Woodward, & Silva, 2005
). In a related fMRI study, a mother's self-report of early experiences with her own mother has been associated with maternal brain responses to infant cries at the first postpartum period (Kim et al., 2010
). Thus, these maternal factors that contribute to each mother's decision to breastfeed, include the strength of the emotional bond with the fetus as well as the sum of early life experiences with her own mother. These factors, in turn, may play a role in both the mother's brain activations and parenting behaviors. The relationship between breastfeeding and parenting may also be moderated by environmental factors such as cultural and socio-economic background as well as other maternal characteristics such as race, education level, and age. Studies have shown that breastfeeding mothers tend to be older, more educated, of higher socioeconomic status, and of greater social support (Dennis, 2002
). In the current study, breastfeeding mothers tended to be more educated. As a result, we included maternal education as a covariate in the analyses. High levels of education, socioeconomic status and social support are also important factors for responsive parenting (Magnuson & Duncan, 2002
; McLoyd & Wilson, 1990
). Society's perception of breastfeeding could also moderate the link between breastfeeding and parental outcomes. In some societies, breastfeeding is the norm of infant feeding practice and breastfeeding may not necessarily predict the quality of maternal care, whereas in other societies breastfeeding may not be strongly encouraged. Thus, future studies are needed to assess whether these confounding maternal and environmental/contextual factors may have affected the choice of feeding styles and contribute to long-term differences in brain activations and parenting behaviors between breastfeeding and bottle-feeding mothers.
Limitations of the study are important to consider in the interpretation of the findings and for guiding future research. First, although our sample is considered sizable for a brain imaging study, the number of mothers who participated in this study is relatively small. Future studies with a larger sample of mothers may be able to tease apart changes related to specific parenting behaviors from those related to non-specific aspects of the early post-partum. Second, although infant cries from the two groups and the control infant cry were rated as having a similar level of emotional intensity by independent raters, because mothers selected samples of their own baby cries by themselves, it is possible that one group of mothers may have selected cry samples which they perceived as being more emotionally salient. Thus, future studies comparing brain responses to three groups of cry stimuli – own baby, other group's baby, and control baby – may help resolve this issue. Third, we did not measure maternal sensitivity at 2-4 weeks postpartum when the brain responses to infant stimuli were assessed. Future studies are needed to explore the relationship between patterns of maternal brain activations and concurrent mother-infant dyadic interaction.
In sum, our findings represent the first evidence using brain imaging that breastfeeding at the first month postpartum has a significant link to both enhanced maternal brain responses to infant stimuli and maternal behaviors. Consistent with these results, we found that the greater maternal brain response to own baby stimuli at the first few weeks of a child's life may be related to more positive and sensitive mothering during the early postpartum period. However, because factors related to a mother's decision to breastfeed may also be associated with these parental outcomes, future research is needed to understand whether breastfeeding moderate the relationship between a mother's decision to breastfeed and neurological responses to her infant with a pre- and post-intervention studies. More research is also required to examine whether the increase in brain response related to breastfeeding and the significant associations between early maternal brain responses and later parenting behaviors influence the infant's cognitive, social, and emotional development.