In addition to interpersonal social ecologies important for understanding sex differences in emotional expression, as discussed by Vigil in the target article, parent-infant interactions are a specific, measurable, and evolutionarily significant arena (Feldman Reference Feldman2007). Indeed, by the third month postpartum, face-to-face, synchronous parent-infant interactions teach infants about a range of emotional social interactions (Feldman et al. Reference Feldman, Greenbaum and Yirmiya1999; Tronick Reference Tronick1989). These early-life interactions consist of brief behavioral units in dyad-specific patterns. One of very few studies that have considered such parent-infant interaction as a function of parental gender (Dickson et al. Reference Dickson, Walker and Fogel1997) examined the co-occurrences of infant smile type and play type during interactions with each parent. During father-child interactions, object-oriented play was more frequent and tended to co-occur with basic smiles, whereas mother-child play included more vocalizations. In another study, time-series analysis of 100 first-time mothers and fathers interacting with their 5-month-old firstborn, coded with 1 second resolution, showed that during play with mother, infants cycled between states of low and medium arousal, often with one peak of high positive emotionality during the engagement episode (Feldman Reference Feldman2003). In this study, mother-child play focused on face-to-face exchange and included patterns of mutual gazing, covocalization, and affectionate touch integrated into timed configurations. In contrast, during play with fathers, the time-line of arousal contained several quick peaks of high positive emotionality, including joint laughter and open exuberance, and individual linear regressions showed that these peaks became more frequent as play proceeded. Furthermore, father-child interactions centered on physical games, or games with an object focus, rather than on attention to micro-level face-to-face signals. This latter finding is consistent with previous research (Lamb Reference Lamb1977; Yogman Reference Yogman1981).

However, despite parent-gender differences in content, no differences were detected in temporal parameters, suggesting that father-infant play may be as synchronous as mother-infant play. Father-son and mother-daughter dyads showed the highest levels of synchrony, with respect to coherence, more mutuality in the lead-lag structure, and shorter time lags to synchrony. It has been suggested that synchrony builds on the infant's biological rhythms and extends it to social relatedness (Lester et al. Reference Lester, Hoffman and Brazelton1985; Wolff Reference Wolff1967). Perhaps female newborns' higher social orientations, increased periods of eye contact, smiles, and rhythmical mouthing contrast with male newborns' frequent peaks of excitement, quicker rapidity of buildup, and higher reflex startling (Korner Reference Korner1969; Osofsky Reference Osofsky1976) to more easily match and build on similar parent interactions that tend to build on these innate dispositions.

Thus, mothers and fathers provide infants two modes of co-regulation. As infants interact with mother and father, they learn that interpersonal intimacy may come in different forms; some relationships focus on subtle shifts in facial signals, whereas others are directed to exploring of the outside world; some are moderate in intensity, whereas others may be more arousing and exciting. Also, some are consistent with the individual's biological tendencies, while others may require some adjustment. As one might expect, it has been shown that mother-son dyads take longer to repair from mismatched to matched states (Weinberg et al. Reference Weinberg, Tronick, Cohn and Olson1999), which may be explained by gender mismatching of dyadic interactions between mother and son. Such experiments explain the well-established link between early father absence and the development of externalizing disorders (Cabrera et al. Reference Cabrera, Tamis-LeMonda, Bradley, Hofferth and Lamb2000).

Since synchrony is central for the development of self-regulation, father absence and lack of sufficient and naturally more synchronous same-gender early interactions may disrupt the acquisition of self-regulatory skills and lead to conduct disorders in boys. This may also point to possible protective therapeutic interventions to maximize opposite-gender parent-infant interactions. These findings fit with psychoanalytic notions that early relational patterns construct person-specific internalized models (Stern Reference Stern1985), perhaps through the development of specific emotion-regulation brain circuits (Leppanen & Nelson Reference Leppanen and Nelson2009), to serve as templates for intimate emotional interactions throughout life (Cassidy & Shaver Reference Cassidy and Shaver2008). Unique contributions from mother-child interaction (Moran et al. Reference Moran, Forbes, Evans, Tarabulsy and Madigan2008) and father-child interaction (Boyce et al. Reference Boyce, Essex, Alkon, Goldsmith, Kraemer and Kupfer2006; Grossmann et al. Reference Grossmann, Grossmann, Fremmer-Bombik, Kindler, Scheuerer-English and Zimmerman2002) to evolutionarily favorable sex-specific emotional expressions of the developing child may significantly constitute the mechanism through which sex differences cross generations.

These sex differences in emotional expression, manifested and perhaps transmitted through parent-infant interactions, are presumably based on sexual differences in parental brain structure and function across species (Bridges Reference Bridges2008) and in humans in particular (Swain & Lorberbaum Reference Swain, Lorberbaum and Bridges2008; Swain et al. Reference Swain, Lorberbaum, Kose and Strathearn2007). Such studies also lie within the larger and growing field addressing sex differences in brain structure, function, and chemistry (Cosgrove et al. Reference Cosgrove, Mazure and Staley2007). For example, neurochemical modulators such as oxytocin and vasopressin (Donaldson & Young Reference Donaldson and Young2008) are likely to be important determinants of emotion expression, as well as contribute to psychopathology risk.

Furthermore, brain networks that differ according to sex likely also vary according to the type of emotional stimuli (Hamann et al. Reference Hamann, Herman, Nolan and Wallen2004; Proverbio et al. Reference Proverbio, Adorni, Zani and Trestianu2009; Schirmer et al. Reference Schirmer, Zysset, Kotz and Yves von Cramon2004; Wager & Ochsner Reference Wager and Ochsner2005), including the involvement of empathys (Schulte-Rüther et al. Reference Schulte-Rüther, Markowitsch, Fink and Piefke2008). For example, considering parent-related stimuli, infant laughing, and crying stimuli versus a control sound, the amygdala and anterior cingulate of non-parent women were more active than those of men (Sander et al. Reference Sander, Frome and Scheich2007). Perhaps these gender-dependent correlates of neural activity reflect neural predispositions in mothers for responses to preverbal infant vocalizations. Direct contrast of men versus women in the first weeks postpartum indicated increased activity in mothers compared with fathers in response to baby cry (Swain et al. Reference Swain, Leckman, Mayes, Feldman, Constable and Schultz2004) and picture (Swain et al. Reference Swain, Leckman, Mayes, Feldman and Schultz2006) in limbic brain regions. This fits with findings that fathers experience more anxious emotional thoughts and engage in more compulsion-like behaviors to reduce their worry (Kim et al., submitted; Leckman et al. Reference Leckman, Mayes, Feldman, Evans, King and Cohen1999; Reference Leckman, Feldman, Swain, Eicher, Thompson and Mayes2004; Swain et al. Reference Swain, Leckman, Mayes, Feldman and Schultz2005). Taken together, this research suggests that networks of highly conserved hypothalamic-midbrain-limbic-paralimbic-cortical circuits act in concert to support aspects of parent response to infants, including the emotion-regulation circuits that vary according to gender. An integrated understanding of the brain basis of parenting according to gender has implications for long-term parent and infant emotional expression and mental health.