The often positive, complex and multifaceted aspects of the smile may be thought to begin with babies in the early postpartum. Perhaps preceding smiling is crying, a signal believed to notify parents to attend to safety, acquire additional resources, and honestly indicate need and vigor (Soltis Reference Soltis2004). Parents will then interact with their infants in cry-care loops (Swain et al. Reference Swain, Mayes and Leckman2004) in order to negotiate their return to contentment. Thus, crying and smiling may be considered as unconditioned responses in babies, to which various forms of conditioning are introduced by the environment – the parents' behaviors in particular – in a gradual, increasingly contingent manner.

The parental capacity to adapt to the postpartum may depend on highly conserved hypothalamic-midbrain-limbic-paralimbic-cortical circuits acting in concert to support parent-response to infants, including the emotion, attention, motivation, empathy, and decision-making to navigate the complexities of parenting – which include baby smile detection, and appropriate responses to prepare that baby for subsequent social settings. For the parent, who typically endures exhaustion and sleep deprivation day-in and day-out alongside the rewarding aspects of care-giving, a baby's smile directed toward a parent has a profound impact on the dyad. A smile, as a signal of fulfillment, serves as a reward that facilitates the interaction synchrony, promotes the sense of relief, fulfillment, and pleasure, strengthens the bonding, and reinforces actions preceding these outcomes in both parties of the dyad. Thus, these smiles within the infant-parent dyad are precursors of all kinds of smiles in adult life. It may be that opiate systems (Panksepp et al. Reference Panksepp, Nelson and Siviy1994) are also important for these hedonic and reinforcing experiences for the dyad. Thus, a repertoire of synchronous dyadic social interactions is developed by about age 3-months in babies, in which infants learn to recognize and respond to the communicative intents of others, share emotions, take turns in a vocal exchange, match the partner's gaze directions and facial expressions, and respond to micro-shifts in attentive states and levels of social involvement (Feldman et al. Reference Feldman, Greenbaum and Yirmiya1999; Tronick Reference Tronick1989) that predicts the nature of future smiling.

The parent-infant dyad is being investigated by several groups – largely from the parent side – using functional neuroimaging during parent experience of baby cry and baby smile among other stimuli, to develop models relevant for parental brain function. This required sensory analysis focuses on brain regions which affect corticolimbic circuits that regulate motivation, reward, and learning about their infant, and ultimately organize parenting impulses, thoughts, and emotions into coordinated behaviors (Swain Reference Swain2008; 2010; Swain & Lorberbaum Reference Swain, Lorberbaum and Bridges2008; Swain et al. Reference Swain, Lorberbaum, Kose and Strathearn2007). Underlining the likely importance of the orbitofrontal cortex (OFC) (raised by Niedenthal et al. in the target article) in responding to a smiling infant (Minagawa-Kawai et al. Reference Minagawa-Kawai, Matsuoka, Dan, Naoi, Nakamura and Kojima2009; Nitschke et al. Reference Nitschke, Nelson, Rusch, Fox, Oakes and Davidson2004), this region also responds to perhaps more ethologically sound stimuli of videotaped baby stimuli (Noriuchi et al. Reference Noriuchi, Kikuchi and Senoo2008). Noriuchi et al. interpreted OFC and related activations as part of circuits required for the execution of well-learned movements. Responses in the OFC may also fit with known significance in reward, punishment, and hedonic experiences in animals and humans (Kringelbach Reference Kringelbach2005), suggesting a lateral-to-medial topographical distribution of negative to positive valence, which is consistent with the aforementioned affiliation-independent OFC activation to both own and others' babies' cries. Notably, Kringelbach (Reference Kringelbach2005) suggested that the OFC loci (BA47/12l) subserve the representation of complex visual reward acquired through learning and memory, which is consistent with findings using own versus others' baby pictures. OFC activity, also reported by Swain et al. (2003) in response to pleasant own-baby pictures could also be interpreted as activation in emotion regulation and habitual behavioral response systems that are active in a range of normal and abnormal emotion-control states, including obsessive-compulsive disorder (Feygin et al. Reference Feygin, Swain and Leckman2006; Leckman & Mayes Reference Leckman and Mayes1999; Swain et al. Reference Swain, Lorberbaum, Kose and Strathearn2007).

In accord with Niedenthal et al., considering that parental response to baby smile may employ empathy and mirror neurons, Lenzi et al. (Reference Lenzi, Trentini, Pantano, Macaluso, Iacoboni, Lenzi and Ammaniti2009) reported that mirror neuron systems, including insula and amygdala, were more active during emotional expressions from a mother's own child, and that they are correlated with maternal reflective function (a measure of empathy). Along the same lines, peripheral oxytocin response to infant contact at 7 months was positively correlated with brain activation in the hormone-regulating hypothalamus and reward-mediating striatum as well as being significantly higher in secure mothers (Strathearn et al. 2009). This strengthens the links between parenting, oxytocin, and reward neurocircuitry that promises to overlap with the rewards of romantic love. Consistent with the importance of oxytocin in regulating social bonds, other recent parent brain neuroimaging papers are linking this hormone with brain activity in response to infant stimuli. Swain and colleagues have found increased activity according to higher oxytocin circumstances of vaginal versus cesarean delivery mode (Swain et al. Reference Swain2008) and breastfeeding versus formula feeding (Kim et al., under review). Taken together, neuroimaging of parents suggest the importance of amygdala, insula, hypothalamus, and striatum, in addition to OFC, for baby-smile response.

Finally, it is interesting to speculate about the long-term impact of some impairment in baby-smile response circuits in parents. This may be part of postpartum depression and the severe adverse effects on children (Feldman & Eidelman Reference Feldman and Eidelman2009; Feldman et al. Reference Feldman, Granat, Pariente, Kanety, Kuint and Gilboa-Schechtman2009) It would be interesting to specifically probe the face response circuits of depressed mothers who are struggling with dyadic interactions. In one attempt to address the effects of early-life events on later parenting, as elaborated in animal models (Kaffman & Meaney Reference Kaffman and Meaney2007), brain structure and function in response to baby stimuli varied according to a measure of perceived maternal care (PMC) (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010). Low PMC was associated with decreased gray matter in the OFC as well as in frontal and superior temporal areas. In addition, functional responses were reduced in nearby cortical areas. Clearly, an integrated understanding of the brain basis of parenting, including smile regulation, has profound implications for long-term parent and infant mental health.