The concept of parent-infant attachment represents a landmark of contemporary developmental psychology (Bowlby Reference Bowlby1969; Reference Bowlby1973). From an evolutionary perspective, attachment represents an innate biological system promoting proximity-seeking between an infant and a conspecific attachment figure. This proximity, rooted in the thoughts and behaviors of parents, then increases the likelihood of infants to survive to reproductive age. Over the last 15 years, brain imaging studies have probed for this parental brain consciousness in health (Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014b) and illness (Moses-Kolko et al. Reference Moses-Kolko, Horner, Phillips, Hipwell and Swain2014) – even beginning to focus on fathers (Swain et al. Reference Swain, Dayton, Kim, Tolman and Volling2014a) – based upon the notion that individual differences in parenting behaviors may be based on variations in neural responses to own versus other baby-cry stimuli. Healthy human mothers are likely to pick up and hold and speak to their infants in response to their infant's cry, and this complex of responsiveness is known to calm an infant (Esposito et al. Reference Esposito, Nakazawa, Venuti and Bornstein2013). Perhaps because of an evolutionary advantage, these parental motor responses are widespread across cultures (Bornstein et al. Reference Bornstein, Tamis-LeMonda, Tal, Ludemann, Toda, Rahn, Pêcheux, Azuma and Vardi1992), neurobiologically embedded (Kim et al. Reference Kim, Strathearn and Swain2016), and are important to understanding consciousness.
Indeed, this work on human parental brain consciousness using own-baby-cry stimuli (Swain et al. Reference Swain, Mayes and Leckman2004) has identified parts of the motor system, pertinent to the work of Morsella et al. in the target article. Indeed, parent brain responses to own versus other baby-cry have included at least two aspects of the motor systems: (1) the pre-supplementary motor area (pre-SMA, Broca's area, superior temporal lobes), known to be involved in the preparation for movement and conscious intention to move (Haggard Reference Haggard2008; Nachev et al. Reference Nachev, Kennard and Husain2008), imagining to grasp (Filimon et al. Reference Filimon, Nelson, Hagler and Sereno2007), experiencing an “urge” to move (Fried et al. Reference Fried, Katz, McCarthy, Sass, Williamson, Spencer and Spencer1991), and preparation for a voice production (Brendel et al. Reference Brendel, Hertrich, Erb, Lindner, Riecker, Grodd and Ackermann2010); and (2) bilateral inferior prefrontal cortices (Broca's areas) associated with social speech processing (Horwitz et al. Reference Horwitz, Amunts, Bhattacharyya, Patkin, Jeffries, Zilles and Braun2003). A recent study further suggested that motor responses to baby-cry may be a function of poverty (Kim et al. Reference Kim, Ho, Evans, Liberzon and Swain2015) underlining the considerable plasticity in parental consciousness systems (Kim et al. Reference Kim, Leckman, Mayes, Feldman, Wang and Swain2010; Reference Kim, Rigo, Mayes, Feldman, Leckman and Swain2014; Reference Kim, Strathearn and Swain2016; Swain Reference Swain2007) according to environment that is itself defined by parenting.
Increasingly sophisticated and ethologically sound stimuli have been used to activate a range of other brain areas that support sensorium to motor output aspects of consciousness. In one of these studies, mothers at 4 to 6 months postpartum were divided into two groups: mothers with highly synchronous maternal behavior scores and low intrusiveness scores (synchronous mothers), and mothers with low synchronous scores and high intrusiveness scores (intrusive mothers) (Atzil et al. Reference Atzil, Hendler and Feldman2011). Synchronous maternal behaviors, including coordination of gaze, touch, and vocalizations with infants, are interpreted as more sensitive parenting behaviors and are associated with positive infant outcomes. Contrariwise, intrusive maternal behaviors include lack of coordination and more directedness with the infant, and they tend to be associated with maternal anxiety and stress responses (Feldman Reference Feldman2007). During a neuroimaging session, mothers were presented with video clips of their own infants and an unfamiliar infant. The main contrast between responses to their own versus the unfamiliar infant was greater activation in the NAcc (Nucleus Accumbens), a key reward/motivation region, and the amygdala, a key stress and negative emotion processing area. When intrusive and synchronous mothers were compared, intrusive mothers showed greater responses in the amygdala to their own babies, whereas synchronous mothers showed greater activation in the NAcc. Furthermore, functional connectivity in the whole brain using the NAcc and the amygdala as seed regions was examined, and the intrusive and synchronous mothers were compared. In synchronous mothers, activity in the NAcc was correlated with activity in attention and social information processing regions, including the inferior frontal gyrus (IFG), the medial frontal gyrus, visual and motor areas, and the parietal cortex. Conversely, intrusive mothers showed greater connectivity between the amygdala and the orbitofrontal cortex (OFC), which is characteristic of elevated anxiety. Thus, reward-related neural responses to one's own infant were associated with enhanced neural connectivity for attention and social information processing, which, in contrast to anxious responses, may support synchronous maternal consciousness.
In another fascinating study of maternal empathy that connects sensory and motor output circuits, mothers observed and imitated faces of their own and other children (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Iacoboni, Lenzi and Ammaniti2009). This study specifically examined the mirror neuron system, localized in the ventral premotor cortex, inferior frontal gyrus (IFG), and posterior parietal cortex, which activates not only when an individual performs an action, but also when observing someone else perform that action. Neural activation in the mirror neuron system was preferentially engaged in response to own child and was correlated with maternal reflective function – sometimes also referred to as mentalization.
Using own versus other baby-cry stimuli, the brain has been studied for possible association with observed maternal mental state talk (Hipwell et al. Reference Hipwell, Guo, Phillips, Swain and Moses-Kolko2015). Prior to the functional magnetic resonance imaging (fMRI) brain scan, mothers were filmed in face-to-face interaction with their 4-month-old infants, and maternal behaviors were blindly and independently coded. Higher functional activity in the right fronto-insular cortex to own versus other baby-cry at the group level, in addition to bilateral subcortical regions including the thalamus, amygdala, hippocampus, and putamen, was positively associated with mental state talk – though, interestingly, not with global aspects of observed caregiving.
Finally, a widespread set of brain responses was reported in a recent study of mothers responding to child visual feedback after a caring decision (Ho et al. Reference Ho, Konrath, Brown and Swain2014). Responses that correlated with dimensions of empathy included the amygdala, ventrolateral prefrontal cortex (PFC), and supplementary motor area that may also fit with broader work on altruism (Brown & Brown Reference Brown and Brown2015; Preston Reference Preston2013; Swain et al. Reference Swain, Konrath, Brown, Finegood, Akce, Dayton and Ho2012) and critically inform progress on consciousness connecting sensory with motor output as aspects.
The concept of parent-infant attachment represents a landmark of contemporary developmental psychology (Bowlby Reference Bowlby1969; Reference Bowlby1973). From an evolutionary perspective, attachment represents an innate biological system promoting proximity-seeking between an infant and a conspecific attachment figure. This proximity, rooted in the thoughts and behaviors of parents, then increases the likelihood of infants to survive to reproductive age. Over the last 15 years, brain imaging studies have probed for this parental brain consciousness in health (Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014b) and illness (Moses-Kolko et al. Reference Moses-Kolko, Horner, Phillips, Hipwell and Swain2014) – even beginning to focus on fathers (Swain et al. Reference Swain, Dayton, Kim, Tolman and Volling2014a) – based upon the notion that individual differences in parenting behaviors may be based on variations in neural responses to own versus other baby-cry stimuli. Healthy human mothers are likely to pick up and hold and speak to their infants in response to their infant's cry, and this complex of responsiveness is known to calm an infant (Esposito et al. Reference Esposito, Nakazawa, Venuti and Bornstein2013). Perhaps because of an evolutionary advantage, these parental motor responses are widespread across cultures (Bornstein et al. Reference Bornstein, Tamis-LeMonda, Tal, Ludemann, Toda, Rahn, Pêcheux, Azuma and Vardi1992), neurobiologically embedded (Kim et al. Reference Kim, Strathearn and Swain2016), and are important to understanding consciousness.
Indeed, this work on human parental brain consciousness using own-baby-cry stimuli (Swain et al. Reference Swain, Mayes and Leckman2004) has identified parts of the motor system, pertinent to the work of Morsella et al. in the target article. Indeed, parent brain responses to own versus other baby-cry have included at least two aspects of the motor systems: (1) the pre-supplementary motor area (pre-SMA, Broca's area, superior temporal lobes), known to be involved in the preparation for movement and conscious intention to move (Haggard Reference Haggard2008; Nachev et al. Reference Nachev, Kennard and Husain2008), imagining to grasp (Filimon et al. Reference Filimon, Nelson, Hagler and Sereno2007), experiencing an “urge” to move (Fried et al. Reference Fried, Katz, McCarthy, Sass, Williamson, Spencer and Spencer1991), and preparation for a voice production (Brendel et al. Reference Brendel, Hertrich, Erb, Lindner, Riecker, Grodd and Ackermann2010); and (2) bilateral inferior prefrontal cortices (Broca's areas) associated with social speech processing (Horwitz et al. Reference Horwitz, Amunts, Bhattacharyya, Patkin, Jeffries, Zilles and Braun2003). A recent study further suggested that motor responses to baby-cry may be a function of poverty (Kim et al. Reference Kim, Ho, Evans, Liberzon and Swain2015) underlining the considerable plasticity in parental consciousness systems (Kim et al. Reference Kim, Leckman, Mayes, Feldman, Wang and Swain2010; Reference Kim, Rigo, Mayes, Feldman, Leckman and Swain2014; Reference Kim, Strathearn and Swain2016; Swain Reference Swain2007) according to environment that is itself defined by parenting.
Increasingly sophisticated and ethologically sound stimuli have been used to activate a range of other brain areas that support sensorium to motor output aspects of consciousness. In one of these studies, mothers at 4 to 6 months postpartum were divided into two groups: mothers with highly synchronous maternal behavior scores and low intrusiveness scores (synchronous mothers), and mothers with low synchronous scores and high intrusiveness scores (intrusive mothers) (Atzil et al. Reference Atzil, Hendler and Feldman2011). Synchronous maternal behaviors, including coordination of gaze, touch, and vocalizations with infants, are interpreted as more sensitive parenting behaviors and are associated with positive infant outcomes. Contrariwise, intrusive maternal behaviors include lack of coordination and more directedness with the infant, and they tend to be associated with maternal anxiety and stress responses (Feldman Reference Feldman2007). During a neuroimaging session, mothers were presented with video clips of their own infants and an unfamiliar infant. The main contrast between responses to their own versus the unfamiliar infant was greater activation in the NAcc (Nucleus Accumbens), a key reward/motivation region, and the amygdala, a key stress and negative emotion processing area. When intrusive and synchronous mothers were compared, intrusive mothers showed greater responses in the amygdala to their own babies, whereas synchronous mothers showed greater activation in the NAcc. Furthermore, functional connectivity in the whole brain using the NAcc and the amygdala as seed regions was examined, and the intrusive and synchronous mothers were compared. In synchronous mothers, activity in the NAcc was correlated with activity in attention and social information processing regions, including the inferior frontal gyrus (IFG), the medial frontal gyrus, visual and motor areas, and the parietal cortex. Conversely, intrusive mothers showed greater connectivity between the amygdala and the orbitofrontal cortex (OFC), which is characteristic of elevated anxiety. Thus, reward-related neural responses to one's own infant were associated with enhanced neural connectivity for attention and social information processing, which, in contrast to anxious responses, may support synchronous maternal consciousness.
In another fascinating study of maternal empathy that connects sensory and motor output circuits, mothers observed and imitated faces of their own and other children (Lenzi et al. Reference Lenzi, Trentini, Pantano, Macaluso, Iacoboni, Lenzi and Ammaniti2009). This study specifically examined the mirror neuron system, localized in the ventral premotor cortex, inferior frontal gyrus (IFG), and posterior parietal cortex, which activates not only when an individual performs an action, but also when observing someone else perform that action. Neural activation in the mirror neuron system was preferentially engaged in response to own child and was correlated with maternal reflective function – sometimes also referred to as mentalization.
Using own versus other baby-cry stimuli, the brain has been studied for possible association with observed maternal mental state talk (Hipwell et al. Reference Hipwell, Guo, Phillips, Swain and Moses-Kolko2015). Prior to the functional magnetic resonance imaging (fMRI) brain scan, mothers were filmed in face-to-face interaction with their 4-month-old infants, and maternal behaviors were blindly and independently coded. Higher functional activity in the right fronto-insular cortex to own versus other baby-cry at the group level, in addition to bilateral subcortical regions including the thalamus, amygdala, hippocampus, and putamen, was positively associated with mental state talk – though, interestingly, not with global aspects of observed caregiving.
Finally, a widespread set of brain responses was reported in a recent study of mothers responding to child visual feedback after a caring decision (Ho et al. Reference Ho, Konrath, Brown and Swain2014). Responses that correlated with dimensions of empathy included the amygdala, ventrolateral prefrontal cortex (PFC), and supplementary motor area that may also fit with broader work on altruism (Brown & Brown Reference Brown and Brown2015; Preston Reference Preston2013; Swain et al. Reference Swain, Konrath, Brown, Finegood, Akce, Dayton and Ho2012) and critically inform progress on consciousness connecting sensory with motor output as aspects.
ACKNOWLEDGMENTS
The authors are supported by the Departments of Psychiatry, Psychology, Center for Human Growth and Development, and Injury Center at the University of Michigan, National Alliance for Research on Schizophrenia and Depression, Klingenstein Third Generation Foundation, NIMHD/NICHD RC2MD004767-01, Michigan Institute for Clinical Health Research and National Center for Advancing Translational Sciences UL1TR000433, and Robert Wood Johnson Health and Society Scholar Award.