Bonding between parents and offspring constitutes the earliest and most influential relationship (Feldman Reference Feldman2007). Building on the work of Bowlby (Reference Bowlby1978), characterizations of this reciprocal interaction between mother and infant and the impact on infant and child development provide powerful theoretical and empirical frameworks within social and developmental psychology (Cassidy & Shaver Reference Cassidy and Shaver1999). Despite increased physiological, emotional, and economical stress (Barclay et al. Reference Barclay, Everitt, Rogan, Schmied and Wyllie1997), both mothers and fathers typically find themselves highly motivated care for their infants' needs (Goodman Reference Goodman2002; Mercer Reference Mercer1985). Sensitive parenting can diminish anxiety and aggression (NICHD Early Care Research Network 2006) and cultivate resilience after stress (Korosi & Baram Reference Korosi and Baram2010). Thus, adults' caregiving for their infants may have roots in early-life experiences with parents (Swain et al. Reference Swain, Konrath, Brown, Finegood and Ho2012). The possibility that maternal behavior depends on the simultaneous regulation of avoidance and approach motivation raises intriguing questions about possible health implications of maternal caregiving because both motivations are tied to the regulation stress response (Brown et al. Reference Brown, Brown, Preston, Brown, Brown and Penner2012). In addition to early-life programming through altered expression of genes in animal models (Champagne Reference Champagne2010), altered brain structure and function in circuitry are directly implicated in the regulation of maternal behavior in humans (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010b). However, reversal of maladaptive brain outcomes with psychotherapy remains to be shown.

Attempts to understand the human maternal brain with brain-imaging studies of mothers listening to baby stimuli highlight an array of emotion response and regulation circuits, including amygdala (alarm), striatum/nucleus accumbens (NA; motivation and reward), and cingulate (decision making). In humans, cortical regions that have not been highlighted so much in the rodent literature have also been described, including the inferior frontal gyrus (IFG), orbitofrontal cortex (OFC), insula, periaqueductal gray (PAG) and dorsomedial prefrontal cortex (dmPFC), that regulate complex social-cognitive functions that are selectively engaged when the maternal brain responds to infant stimuli. (For reviews, see Barrett & Fleming Reference Barrett and Fleming2011; Swain Reference Swain2011.) Direct studies of baby brain structure and function in response to parenting cues have not been done; however, a pioneering neuroimaging study of mothers showed how perceived maternal care (a proxy for the animal models' licking and grooming behaviors) affects both brain structures and functional response to own-baby cries (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010b). In this study, mothers who reported higher maternal care in their own childhood showed higher gray-matter density, proportional to the number of neurons, in a range of higher cortical areas and executive function areas, including the insula, superior and middle frontal gyri, orbital gyrus, superior temporal gyrus, and fusiform gyrus. There were also increased functional responses in a number of frontal brain regions and the insula in response to own-baby cries.

Besides the distant effects of mothers' own early-life experiences, the transition to parenthood also involves maternal brain plasticity around childbirth. In the first prospective longitudinal study of gray-matter changes over the first few months of motherhood, gray-matter volume of the insula, prefrontal cortex, parietal lobes, and midbrain areas between 2–4 weeks and 3–4 months postpartum increased (Kim et al. Reference Kim, Leckman, Mayes, Feldman, Wang and Swain2010a). Furthermore, greater gray-matter volume in the midbrain (including the hypothalamus, substantia nigra, and amygdala) was associated with maternal positive perceptions of her baby. In contrast, the associated chronic stress of low socioeconomic status (SES) involve the amygdala, hippocampus, and PFC (Hackman et al. Reference Hackman, Farah and Meaney2010; McEwen & Gianaros Reference McEwen and Gianaros2010). Also, young adults' recollection of lower SES from their own childhood was reported to be associated with greater amygdala reactivity to threatening but not nonthreatening faces (Gianaros et al. Reference Gianaros, Horenstein, Hariri, Sheu, Manuck, Matthews and Cohem2008). Interestingly, current levels of perceived SES were unrelated to amygdala reactivity to threatening face stimuli – only perceived SES in childhood mattered. Indeed, low-SES parents are themselves more likely to exhibit harsh or unresponsive parenting toward their children, and poverty is also associated with a higher incidence of child abuse and neglect (Conger & Donnellan Reference Conger and Donnellan2007; McLoyd Reference McLoyd1998). Low-quality parenting is furthermore associated with altered neurological development, as evidenced by the effects of early-parental care on hippocampus structure. In humans, adults who experienced adverse parenting during their own childhood have significantly smaller hippocampus volumes in adulthood (Buss et al. Reference Buss, Lord, Wadiwalla, Hellhammer, Lupien, Meaney and Pruessner2007; Woon & Hedges Reference Woon and Hedges2008). However, these studies have not included direct measures of childhood poverty, participants' experiences of either concurrent of childhood chronic stress, or the experience of parenting behaviors. Adults with lower subjective social status had reduced gray-matter volume in the perigenual anterior cingulate cortex (ACC) region of the PFC (Gianaros et al. Reference Gianaros, Horenstein, Cohen, Matthews, Brown, Flory, Critchley, Manuck and Hariri2007). These environmentally sensitive brain regions are involved in many cognitive and emotional regulatory functions, including the appraisal of salient events and emotional experiences, as well as the complex behaviors and possibly cardiovascular reactivity in response to environmental demands (Evans Reference Evans2003; McEwen & Gianaros Reference McEwen and Gianaros2010).

Harsh early-childhood parenting environments also show high amygdala reactivity during an emotion labeling task, positively correlated with high right-ventrolateral-prefrontal-cortex (rvlPFC) activity (Taylor et al. Reference Taylor, Eisenberger, Saxbe, Lehman and Lieberman2006). This can be potentially interpreted as decreased ability of rvlPFC to modulate amygdala activation. Along the same lines, exposure to parental corporal punishment in childhood is associated with reduced gray-matter volume in mPFC, dorsolateral-PFC, and ACC (Tomoda et al. Reference Tomoda, Suzuki, Rabi, Sheu, Polcari and Teicher2009). On the other hand, lower social status may result in increased sensitivity of mentalization circuits some circuits (Muscatell et al. Reference Muscatell, Morelli, Falk, Way, Pfeifer, Galinsky, Lieberman, Dapretto and Eisenberger2012). Despite a growing literature on the brain physiology important for parenting (Swain Reference Swain2011), it remains to be shown how the chronic stress of poverty affects these circuits longitudinally. The environmental role of the father brain is also just beginning to be examined (Swain et al., under review). Recent studies demonstrate epigenetic paternal effects (Chong et al. Reference Chong, Vickaryous, Ashe, Zamudio, Youngson, Hemley, Stopka, Skoultchi, Mathews, Scott, de Kretser, O'Bryan, Blewitt and Whitelaw2007), including the transmission of stress-induced pathologies such as depression (Dietz et al. Reference Dietz, Laplant, Watts, Hodes, Russo, Feng, Oosting, Vialou and Nestler2011; Dietz & Nestler Reference Dietz and Nestler2012). The effects of early-experience on the developing brain for emotion regulation may be further linked to next generations' capacity for sensitive parental behaviors (Francis et al., Reference Francis, Diorio, Liu and Meaney1999; Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010b; Meaney Reference Meaney2001) with resulting implications for public policy (Dawson et al. Reference Dawson, Ashman and Carver2000).