Parenting is a specific example of teaching that serves in the construction of infant self-representation (Fonagy et al. Reference Fonagy, Gergely and Target2007). In this conceptualization, infants possess an innate contingency detector, which orients them towards aspects of the social world that react congruently and in a specifically cued informative manner that expresses and facilitates the learning of cultural knowledge. Thus, the infant focuses on the attachment figure – usually the parent – as a source of reliable information about the world. The infant then is taught about the world through the caregiver's pedagogical communicative displays which focus on the child's thoughts and feelings. We argue that a number of possible mechanisms – rooted in neurohormonal systems in parents and amenable to study – inform the mentalistic, cultural, and functional definitions of teaching reviewed by Kline in the target article.
In mentalistic definitions of teaching, Kline reviews the necessity for theory of mind (ToM) capacities for teaching, which are well established to be crucial to the neurohormonal basis of parenting (Swain et al. Reference Swain, Kim and Ho2011; Reference Swain, Konrath, Brown, Finegood, Akce, Dayton and Ho2012). The importance of early postpartum cry–care loops, that is, cycles of communication and response between infant and parent (Swain et al. Reference Swain, Mayes and Leckman2004), stimulated research using poignant baby-cry stimuli to activate parent brains. This line of investigation has outlined the importance of brain circuits and key hormones involved in empathy or ToM and emotion regulation in both mothers and fathers; and suggests a framework for understanding how these circuits function or malfunction, and how they could be optimized with brain-based interventions that may be applied to improve teacher performance and student outcomes (Swain & Lorberbaum Reference Swain, Lorberbaum and Bridges2008; Swain et al. Reference Swain, Dayton, Kim, Tolman and Volling2014a; Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014c).
One of the key conceptualizations in the neuroscience of parenting has been that of ToM (Mahy et al. Reference Mahy, Moses and Pfeifer2014) – closely related to empathy, which has been a central topic in social neuroscience highlighting the insula (Decety Reference Decety2015; Lamm et al. Reference Lamm, Batson and Decety2007). Among parents, the insula was activated while they reacted to their own babies crying (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010), and was more activated among breastfeeding mothers than among formula feeding mothers (Kim et al. Reference Kim, Feldman, Mayes, Eicher, Thompson, Leckman and Swain2011). Furthermore, observing and actually imitating the faces of their own children revealed activations in the insula and other cortical motor imitation and mirror neuron systems (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Iacoboni, Lenzi and Ammaniti2009), with activation correlated positively with levels of maternal empathy assessed by means of independent validated interviews. Support for the insula being part of a general system of empathy includes responses of non-parents to baby pictures (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Lenzi and Ammaniti2013) – which also involves pre-motor cortex activation in preparation for appropriate behavioral responses (Caria et al. Reference Caria, Falco, Venuti, Lee, Esposito, Rigo, Birbaumer and Bornstein2012) that partially cross cultures (Bornstein et al., under review). This is in accord with the culture-based aspects of teaching discussed by Kline in the target article, and elaborated for parenting (Bornstein Reference Bornstein2013).
In accord with the functionalist approaches mentioned by Kline, parenting in nonhuman animals may also serve as an informative model for teaching. For rhesus macaques who have recently been shown to engage in parenting activity homologous to humans (Ferrari et al. Reference Ferrari, Paukner, Ionica and Suomi2009), about 50% of infants engage in neonatal imitation of lip-smacking and tongue protrusion gestures (Simpson et al. Reference Simpson, Paukner, Suomi and Ferrari2014a). This appears to be under hormone control similar to humans (Simpson et al. Reference Simpson, Sclafani, Paukner, Hamel, Novak, Meyer, Suomi and Ferrari2014b), with implications for later infant capacity for eye-contact (Simpson et al. Reference Simpson, Paukner, Suomi and Ferrari2014a) underlining the evolutionary soundness of teaching behaviors that cross species in the instance of parenting.
Direct studies of reciprocal baby brain function in response to their parents are yet to be done; however, a recent neuroimaging study of mothers showed how perceived maternal care (a proxy for animal models' licking and grooming behaviors) affects both brain structures and functional response to their babies' cries in adult mothers (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010). 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 their own babies' cries. This may reflect the long-term effects in humans of early-life mother–child interactions affecting adult maternal mother–infant interactions.
Recently, two studies of maternal interactions with brief video clips come closest to simulating the direct interaction of teaching for parents. In one study, mothers were scanned while observing several of their own as well as standard infant-related vignettes (Atzil et al. Reference Atzil, Hendler and Feldman2011). Beyond basic motivation/reward (nucleus accumbens [NA]) responses, the functional NA and amygdala were functionally correlated with emotion modulation, ToM, and empathy networks, including the insula. New paradigms include decision-making tasks, in which parental brain response to infant feedback tracks empathy measures inversely according to stress responsivity as indexed by cortisol measurements (Ho et al. Reference Ho, Konrath, Brown and Swain2014).
Positive feelings about their infants and parenting experience maybe critical in pathways engaging the dopamine-oxytocin reward circuits described in animal models (MacDonald Reference MacDonald1992; Numan & Insel Reference Numan and Insel2003; Shahrokh et al. Reference Shahrokh, Zhang, Diorio, Gratton and Meaney2010). Thus, interactions with the infant may enhance parental oxytocin and dopamine release and foster the maintenance of positive parental behaviors with associated attentiveness and sensitive caregiving – perhaps implicating future therapeutic potential (Macdonald et al. Reference Macdonald, Macdonald, Brune, Lamb, Wilson, Golshan and Feifel2013). In contrast, if interactions with the infant are negative and stressful, parents may experience less brain activation in reward-motivation pathways, find the relationship less satisfying, harbor fewer positive parental thoughts, and be less willing to maintain those interactions – as may be more common with mental illnesses such as postpartum depression.
We finally touch on the issues of mental illness affecting the teaching function of parents. Postpartum depression is associated with deficits in parenting (Feldman et al. Reference Feldman, Granat, Pariente, Kanety, Kuint and Gilboa-Schechtman2009) – this may be conceived as an illness of teaching. Ongoing research on the brain function in postpartum depression suggests impairments in specific empathy and emotion regulation circuits (Moses-Kolko et al. Reference Moses-Kolko, Hipwell and Swain2014) that may be amenable to intervention (see Swain et al. Reference Swain, Ho, Dayton, Rosenblum and Muzik2014b).
Parenting is a specific example of teaching that serves in the construction of infant self-representation (Fonagy et al. Reference Fonagy, Gergely and Target2007). In this conceptualization, infants possess an innate contingency detector, which orients them towards aspects of the social world that react congruently and in a specifically cued informative manner that expresses and facilitates the learning of cultural knowledge. Thus, the infant focuses on the attachment figure – usually the parent – as a source of reliable information about the world. The infant then is taught about the world through the caregiver's pedagogical communicative displays which focus on the child's thoughts and feelings. We argue that a number of possible mechanisms – rooted in neurohormonal systems in parents and amenable to study – inform the mentalistic, cultural, and functional definitions of teaching reviewed by Kline in the target article.
In mentalistic definitions of teaching, Kline reviews the necessity for theory of mind (ToM) capacities for teaching, which are well established to be crucial to the neurohormonal basis of parenting (Swain et al. Reference Swain, Kim and Ho2011; Reference Swain, Konrath, Brown, Finegood, Akce, Dayton and Ho2012). The importance of early postpartum cry–care loops, that is, cycles of communication and response between infant and parent (Swain et al. Reference Swain, Mayes and Leckman2004), stimulated research using poignant baby-cry stimuli to activate parent brains. This line of investigation has outlined the importance of brain circuits and key hormones involved in empathy or ToM and emotion regulation in both mothers and fathers; and suggests a framework for understanding how these circuits function or malfunction, and how they could be optimized with brain-based interventions that may be applied to improve teacher performance and student outcomes (Swain & Lorberbaum Reference Swain, Lorberbaum and Bridges2008; Swain et al. Reference Swain, Dayton, Kim, Tolman and Volling2014a; Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014c).
One of the key conceptualizations in the neuroscience of parenting has been that of ToM (Mahy et al. Reference Mahy, Moses and Pfeifer2014) – closely related to empathy, which has been a central topic in social neuroscience highlighting the insula (Decety Reference Decety2015; Lamm et al. Reference Lamm, Batson and Decety2007). Among parents, the insula was activated while they reacted to their own babies crying (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010), and was more activated among breastfeeding mothers than among formula feeding mothers (Kim et al. Reference Kim, Feldman, Mayes, Eicher, Thompson, Leckman and Swain2011). Furthermore, observing and actually imitating the faces of their own children revealed activations in the insula and other cortical motor imitation and mirror neuron systems (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Iacoboni, Lenzi and Ammaniti2009), with activation correlated positively with levels of maternal empathy assessed by means of independent validated interviews. Support for the insula being part of a general system of empathy includes responses of non-parents to baby pictures (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Lenzi and Ammaniti2013) – which also involves pre-motor cortex activation in preparation for appropriate behavioral responses (Caria et al. Reference Caria, Falco, Venuti, Lee, Esposito, Rigo, Birbaumer and Bornstein2012) that partially cross cultures (Bornstein et al., under review). This is in accord with the culture-based aspects of teaching discussed by Kline in the target article, and elaborated for parenting (Bornstein Reference Bornstein2013).
In accord with the functionalist approaches mentioned by Kline, parenting in nonhuman animals may also serve as an informative model for teaching. For rhesus macaques who have recently been shown to engage in parenting activity homologous to humans (Ferrari et al. Reference Ferrari, Paukner, Ionica and Suomi2009), about 50% of infants engage in neonatal imitation of lip-smacking and tongue protrusion gestures (Simpson et al. Reference Simpson, Paukner, Suomi and Ferrari2014a). This appears to be under hormone control similar to humans (Simpson et al. Reference Simpson, Sclafani, Paukner, Hamel, Novak, Meyer, Suomi and Ferrari2014b), with implications for later infant capacity for eye-contact (Simpson et al. Reference Simpson, Paukner, Suomi and Ferrari2014a) underlining the evolutionary soundness of teaching behaviors that cross species in the instance of parenting.
Direct studies of reciprocal baby brain function in response to their parents are yet to be done; however, a recent neuroimaging study of mothers showed how perceived maternal care (a proxy for animal models' licking and grooming behaviors) affects both brain structures and functional response to their babies' cries in adult mothers (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010). 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 their own babies' cries. This may reflect the long-term effects in humans of early-life mother–child interactions affecting adult maternal mother–infant interactions.
Recently, two studies of maternal interactions with brief video clips come closest to simulating the direct interaction of teaching for parents. In one study, mothers were scanned while observing several of their own as well as standard infant-related vignettes (Atzil et al. Reference Atzil, Hendler and Feldman2011). Beyond basic motivation/reward (nucleus accumbens [NA]) responses, the functional NA and amygdala were functionally correlated with emotion modulation, ToM, and empathy networks, including the insula. New paradigms include decision-making tasks, in which parental brain response to infant feedback tracks empathy measures inversely according to stress responsivity as indexed by cortisol measurements (Ho et al. Reference Ho, Konrath, Brown and Swain2014).
Positive feelings about their infants and parenting experience maybe critical in pathways engaging the dopamine-oxytocin reward circuits described in animal models (MacDonald Reference MacDonald1992; Numan & Insel Reference Numan and Insel2003; Shahrokh et al. Reference Shahrokh, Zhang, Diorio, Gratton and Meaney2010). Thus, interactions with the infant may enhance parental oxytocin and dopamine release and foster the maintenance of positive parental behaviors with associated attentiveness and sensitive caregiving – perhaps implicating future therapeutic potential (Macdonald et al. Reference Macdonald, Macdonald, Brune, Lamb, Wilson, Golshan and Feifel2013). In contrast, if interactions with the infant are negative and stressful, parents may experience less brain activation in reward-motivation pathways, find the relationship less satisfying, harbor fewer positive parental thoughts, and be less willing to maintain those interactions – as may be more common with mental illnesses such as postpartum depression.
We finally touch on the issues of mental illness affecting the teaching function of parents. Postpartum depression is associated with deficits in parenting (Feldman et al. Reference Feldman, Granat, Pariente, Kanety, Kuint and Gilboa-Schechtman2009) – this may be conceived as an illness of teaching. Ongoing research on the brain function in postpartum depression suggests impairments in specific empathy and emotion regulation circuits (Moses-Kolko et al. Reference Moses-Kolko, Hipwell and Swain2014) that may be amenable to intervention (see Swain et al. Reference Swain, Ho, Dayton, Rosenblum and Muzik2014b).
ACKNOWLEDGMENTS
The authors are supported by the Department of Psychiatry, Psychology and Injury Center (Centers for Disease Control & Prevention Award Number U49/CE002099) at the University of Michigan; National Alliance for Research on Schizophrenia and Depression; Klingenstein Third Generation Foundation; NIMHD/NICHD grant RC2MD004767-01; Michigan Institute for Clinical Health Research and National Center for Advancing Translational Sciences grant UL1TR000433; and Robert Wood Johnson Health and Society Scholar Award.