Parental reflective functioning and the neural correlates of processing infant affective cues

Parental reflective functioning refers to the capacity for a parent to understand their own and their infant’s mental states, and how these mental states relate to behavior. Higher levels of parental reflective functioning may be associated with greater sensitivity to infant emotional signals in fostering adaptive and responsive caregiving. We investigated this hypothesis by examining associations between parental reflective functioning and neural correlates of infant face and cry perception using event-related potentials (ERPs) in a sample of recent mothers. We found both early and late ERPs were associated with different components of reflective functioning. These findings suggest that parental reflective functioning may be associated with the neural correlates of infant cue perception and further support the value of enhancing reflective functioning as a mechanism in parenting intervention programs.     

Parity and neural responses to social and non-social stimuli in pregnancy

ABSTRACT

Prior reproductive experience, or parity, may contribute to differential neural responses to infant stimuli during pregnancy. We examined the P300 elicited by viewing infant and adult faces, as well as houses, in women pregnant with their first child and compared their neural responses to women who had at least one child prior to their current pregnancy. We found the P300 amplitude was larger in women pregnant with their first child as compared to pregnant women who had previously had children. This larger P300 was observed in response to all visual stimuli and was not specific to infant faces. Taken together, these findings indicate increased sensitivity toward social and non-social stimuli in pregnancy and indicate the importance of measuring parity in social neuroscience studies of pregnancy and motherhood.     

Depression symptomatology and the neural correlates of infant face and cry perception during pregnancy

Depression symptoms during pregnancy may affect emerging maternal sensitivity and have lasting consequences for the dyadic relationship. Here, we examined whether depression was associated with the neural correlates of infant face and cry perception during pregnancy. In 36 women between 34 and 38 weeks gestation, we examined the P300 elicited by infant emotional (happy, distressed, and neutral) faces and cries (high- and low-distress cries and a neutral tone). The Edinburgh Postnatal Depression Scale and the Beck Depression Inventory-II were employed to measure current depression symptomatology. Higher depression symptoms were associated with an attenuated P300 to distressed infant faces, but not with happy or neutral infant faces. There was no association between depression symptoms and the P300 elicited by infant cries. These results suggest that depression symptoms during pregnancy may affect neural processing of infant faces, especially when the infant face is expressing distress.     

Covert recognition and the neural system for face processing

In this viewpoint, we discuss the new evidence on covert face recognition in prosopagnosia presented by Bobes et al. (2003, this issue) and by Sperber and Spinnler (2003, this issue). Contrary to earlier hypotheses, both papers agree that covert and overt face recognition are based on the same mechanism. In line with this suggestion, an analysis of reported cases with prosopagnosia indicates that a degree of successful encoding of facial representations is a prerequisite for covert recognition to occur. While we agree with this general conclusion as far as Bobes et al.'s and Sperber and Spinnler's data are concerned, we also discuss evidence for a dissociation between different measures of covert recognition. Specifically, studies in patients with Capgras delusion and patients with prosopagnosia suggest that skin conductance and behavioural indexes of covert face recognition are mediated by partially different mechanisms. We also discuss implications of the new data for models of normal face recognition that have been successful in simulating covert recognition phenomena (e.g., Young and Burton, 1999, and O'Reilly et al., 1999). Finally, in reviewing recent neurophysiological and brain imaging evidence concerning the neural system for face processing, we argue that the relationship between ERP components (specifically, N170, N250r, and N400) and different cognitive processes in face recognition is beginning to emerge.     

Gender and parental status affect the visual cortical response to infant facial expression

This study sought to determine the influence of gender and parental status on the brain potentials elicited by viewing infant facial expressions. We used ERP recording during a judgement task of infant happy/distressed expression to investigate if viewer gender or parental status affects the visual cortical response at various stages of perceptual processing. ERPs were recorded in 38 adults (male/female, parents/non-parents) during processing of infant facial expressions that varied in valence and intensity. All infants were unfamiliar to viewers. The lateral occipital P110 response was much larger in women than in men, regardless of facial expression, thus indicating a gender difference in early visual processing. The occipitotemporal N160 response provided the first evidence of discrimination of expressions of discomfort and distress and demonstrated a significant gender difference within the parent group, thus suggesting a strong interactive influence of genetic predisposition and parental status on the responsivity of visual brain areas. The N245 component exhibited complete coding of the intensity of facial expression, including positive expressions. At this processing stage the cerebral responses of female and male non-parents were significantly smaller than those of parents and insensitive to differences in the intensity of infant suffering. Smaller P300 amplitudes were elicited in mothers versus fathers, especially with infant expressions of suffering. No major group differences were observed in cerebral responses to happy or comfortable expressions. These findings suggest that mere familiarity with infant faces does not explain group differences.     

Associations between maternal negative affect and adolescent's neural response to peer evaluation

Parenting is often implicated as a potential source of individual differences in youths’ emotional information processing. The present study examined whether parental affect is related to an important aspect of adolescent emotional development, response to peer evaluation. Specifically, we examined relations between maternal negative affect, observed during parent–adolescent discussion of an adolescent-nominated concern with which s/he wants parental support, and adolescent neural responses to peer evaluation in 40 emotionally healthy and depressed adolescents. We focused on a network of ventral brain regions involved in affective processing of social information: the amygdala, anterior insula, nucleus accumbens, and subgenual anterior cingulate, as well as the ventrolateral prefrontal cortex. Maternal negative affect was not associated with adolescent neural response to peer rejection. However, longer durations of maternal negative affect were associated with decreased responsivity to peer acceptance in the amygdala, left anterior insula, subgenual anterior cingulate, and left nucleus accumbens. These findings provide some of the first evidence that maternal negative affect is associated with adolescents’ neural processing of social rewards. Findings also suggest that maternal negative affect could contribute to alterations in affective processing, specifically, dampening the saliency and/or reward of peer interactions during adolescence.     

Investigating the impact of parental status and depression symptoms on the early perceptual coding of infant faces: An event-related potential study

Infant faces are highly salient social stimuli that appear to elicit intuitive parenting behaviors in healthy adult women. Behavioral and observational studies indicate that this effect may be modulated by experiences of reproduction, caregiving, and psychiatric symptomatology that affect normative attention and reward processing of infant cues. However, relatively little is known about the neural correlates of these effects. Using the event-related potential (ERP) technique, this study investigated the impact of parental status (mother, non-mother) and depression symptoms on early visual processing of infant faces in a community sample of adult women. Specifically, the P1 and N170 ERP components elicited in response to infant face stimuli were examined. While characteristics of the N170 were not modulated by parental status, a statistically significant positive correlation was observed between depression symptom severity and N170 amplitude. This relationship was not observed for the P1. These results suggest that depression symptoms may modulate early neurophysiological responsiveness to infant cues, even at sub-clinical levels.     

Ready for action: a role for the human midbrain in responding to infant vocalizations

Infant vocalizations are among the most biologically salient sounds in the environment and can draw the listener to the infant rapidly in both times of distress and joy. A region of the midbrain, the periaqueductal gray (PAG), has long been implicated in the control of urgent, survival-related behaviours. To test for PAG involvement in the processing of infant vocalizations, we recorded local field potentials from macroelectrodes implanted in this region in four adults who had undergone deep brain stimulation. We found a significant difference occurring as early as 49 ms after hearing a sound in activity recorded from the PAG in response to infant vocalizations compared with constructed control sounds and adult and animal affective vocalizations. This difference was not present in recordings from thalamic electrodes implanted in three of the patients. Time frequency analyses revealed distinct patterns of activity in the PAG for infant vocalisations, constructed control sounds and adult and animal vocalisations. These results suggest that human infant vocalizations can be discriminated from other emotional or acoustically similar sounds early in the auditory pathway. We propose that this specific, rapid activity in response to infant vocalizations may reflect the initiation of a state of heightened alertness necessary to instigate protective caregiving.     

Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development

Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on neural (EEG) and behavioral responses during observation of live facial gestures in infant macaques with limited social exposure (i.e. nursery-reared). Three key findings were revealed. First, OT increased alpha suppression over posterior scalp regions during observation of facial gestures but not non-biological movement, suggesting that OT targets self-other matching and attentional cortical networks involved in social perception from very early infancy. Second, OT increased infant production of matching facial gestures and attention towards the most socially-relevant facial stimuli, both behaviors typically silenced by early social deprivation. Third, infants with higher cortisol levels appeared to benefit the most from OT, displaying greater improvements in prosocial behaviors after OT administration. Altogether, these findings suggest that OT promotes prosocial behaviors and associated neural responses likely impacted by early social adversity, and demonstrate the potential of OT administration to ameliorate social difficulties in the context of neurodevelopmental and early-emerging psychiatric disorders, at a developmental stage when brain plasticity is greatest.     

Reported maternal childhood maltreatment experiences,amygdala activation and functional connectivity to infant cry

Maternal childhood maltreatment experiences (CMEs) may influence responses to infants and affect child outcomes. We examined associations between CME and mothers’ neural responses and functional connectivity to infant distress. We hypothesized that mothers with greater CME would exhibit higher amygdala reactivity and amygdala–supplementary motor area (SMA) functional connectivity to own infant’s cries. Postpartum mothers (N = 57) assessed for CME completed an functional magnetic resonance imaging task with cry and white-noise stimuli. Amygdala region-of-interest and psychophysiological interaction analyses were performed. Our models tested associations of CME with activation and connectivity during task conditions (own/other and cry/noise). Exploratory analyses with parenting behaviors were performed. Mothers with higher CME exhibited higher amygdala activation to own baby’s cries vs other stimuli (F_1,392 = 6.9, P < 0.01, N = 57) and higher differential connectivity to cry vs noise between amygdala and SMA (F_1,165 = 22.3, P < 0.001). Exploratory analyses revealed positive associations between both amygdala activation and connectivity and maternal non-intrusiveness (Ps < 0.05). Increased amygdala activation to own infant’s cry and higher amygdala–SMA functional connectivity suggest motor responses to baby’s distress. These findings were associated with less intrusive maternal behaviors. Follow-up studies might replicate these findings, add more granular parenting assessments and explore how cue processing leads to a motivated maternal approach in clinical populations.     

A walk on the dark side: TMS over the right inferior frontal gyrus (rIFG) disrupts behavioral responses to infant stimuli

ABSTRACT

Infant signals, including infant sounds and facial expressions, play a critical role in eliciting parental proximity and care. Processing of infant signals in the adulthood brain is likely to recruit emotional empathy neural circuits, including the inferior frontal gyrus (IFG). Here, we used transcranial magnetic stimulation (TMS) to test the role of right IFG (rIFG) in behavioral responses to infant signals. Specifically, a group of nulliparous women were asked to perform a handgrip dynamometer task and an Approach-Avoidance Task (AAT) after receiving TMS over the right IFG or over a control site (vertex). Suppressing activity in the rIFG affected the modulation of handgrip force in response to infant crying. Moreover, the AAT showed that participants tend to avoid the sad infant face after Vertex stimulation, and this bias was counteracted by rIFG stimulation. Our results suggest a causal role of rIFG in sensitive responding towards sad infants and point to the rIFG as a critical node in the neural network underlying the innate releasing mechanism for feelings of love, affection and caring of sad infants.     

Maternal sensitivity and infant neural response to touch: an fNIRS study

The mother’s attunement to her infant’s emotional needs influences her use of touching behaviors during mother–infant interactions. Moreover, maternal touch appears to modulate infants’ physiological responses to affective touch. However, little is known about the impact of maternal sensitivity on infants’ touch processing at a brain level. This study explored the association between maternal sensitivity when infants (N = 24) were 7 months old and their patterns of cortical activation to touch at 12 months. Brain activation was measured using functional near-infrared spectroscopy. Changes in oxy-hemoglobin (HbO₂) and deoxy-hemoglobin (HHb) concentrations were measured in the left somatosensory cortex and right temporal cortex while infants received two types of tactile stimulation—affective and discriminative touch. Results showed that a lower maternal sensitivity was associated with a higher HbO₂ response for discriminative touch over the temporal region. Additionally, infants of less sensitive mothers tended to present a higher response in HbO₂ for affective touch over the somatosensory region. These findings suggest that less sensitive interactions might result in a lower exposure to maternal touch, which can be further related to infants’ neural processing of touch.     

Behavioral and genetic correlates of the neural response to infant crying among human fathers

Although evolution has shaped human infant crying and the corresponding response from caregivers, there is marked variation in paternal involvement and caretaking behavior, highlighting the importance of understanding the neurobiology supporting optimal paternal responses to cries. We explored the neural response to infant cries in fathers of children aged 1–2, and its relationship with hormone levels, variation in the androgen receptor (AR) gene, parental attitudes and parental behavior. Although number of AR CAG trinucleotide repeats was positively correlated with neural activity in brain regions important for empathy (anterior insula and inferior frontal gyrus), restrictive attitudes were inversely correlated with neural activity in these regions and with regions involved with emotion regulation (orbitofrontal cortex). Anterior insula activity had a non-linear relationship with paternal caregiving, such that fathers with intermediate activation were most involved. These results suggest that restrictive attitudes may be associated with decreased empathy and emotion regulation in response to a child in distress, and that moderate anterior insula activity reflects an optimal level of arousal that supports engaged fathering.     

The association of major depression, conduct disorder, and maternal overcontrol with a failure to show a cortisol buffered response in 4-month-old infants of teenage mothers.

BACKGROUND: Adolescent pregnancy can be associated with major depression (MD) and conduct disorder (CD). Some infants of adolescent mothers are prenatally exposed to these factors, which may result in heightened risk for perturbations of their stress systems. Between 2 and 4 months, a normal shift occurs in the adrenocortical system in which we observe a marked decrease in infant cortisol response when facing mild stressors. This study aimed to explore whether MD (lifetime, during pregnancy, postpartum), CD, and maternal overcontrol are associated with increased cortisol reactivity in 4-month-old infants of teenage mothers. METHODS: Using arm restraint as a stressor, morning salivary cortisol was taken prestressor and poststressor in 212 infants during a laboratory visit. Major depression and CD were measured with the computerized National Institute of Mental Health Diagnostic Interview Schedule (NIMH-DIS), postpartum depressive mood was measured with the Edinburgh Postnatal Depression Scale, and overcontrol was observed with the CARE-Index. RESULTS: Independent of the predictors, there was a dampened cortisol response. Infants of mothers with lifetime MD and of average to highly overcontrolling mothers showed increased cortisol reactivity. Conduct disorder and cortisol levels were not associated. CONCLUSIONS: Future studies should detect whether the absence of a dampened cortisol response in infants whose mothers have lifetime MD or display overcontrolling parenting is stable over time.     

Storing maternal memories: Hypothesizing an interaction of experience and estrogen on sensory cortical plasticity to learn infant cues

Much of the literature on maternal behavior has focused on the role of infant experience and hormones in a canonical subcortical circuit for maternal motivation and maternal memory. Although early studies demonstrated that the cerebral cortex also plays a significant role in maternal behaviors, little has been done to explore what that role may be. Recent work though has provided evidence that the cortex, particularly sensory cortices, contains correlates of sensory memories of infant cues, consistent with classical studies of experience-dependent sensory cortical plasticity in non-maternal paradigms. By reviewing the literature from both the maternal behavior and sensory cortical plasticity fields, focusing on the auditory modality, we hypothesize that maternal hormones (predominantly estrogen) may act to prime auditory cortical neurons for a longer-lasting neural trace of infant vocal cues, thereby facilitating recognition and discrimination. This couldthen more efficiently activate the subcortical circuit to elicit and sustain maternal behavior.     

Electrocortical evidence of increased post-reappraisal neural reactivity and its link to depressive symptoms

Few studies have examined whether effortful emotion regulation has a protracted impact on subsequent affective appraisal, and even fewer have investigated this effect on a trial-by-trial basis. In this study, we hypothesized that engaging cognitive resources via reappraisal during a trial would result in a subsequent period of increased reactivity on the next trial, as quantified using event-related potentials and oscillations. Forty-eight healthy individuals passively viewed unpleasant and neutral pictures followed by an auditory instruction to either continue viewing normally or reappraise emotional response to pictures. Viewing unpleasant pictures yielded increased late positive potential (LPP) and decreased posterior alpha (8–13 Hz) compared with neutral pictures. A similar pattern was observed on trials that immediately ‘followed’ emotion regulation instructions. Moreover, individuals with increased self-reported depressive symptoms showed greater LPP and alpha modulation following emotion regulation, suggesting that these responses may relate to compromised emotion regulation ability. This study demonstrates that cognitive reappraisal induces subsequent heightened reactivity that may reflect transient resource depletion, and these effects are more pronounced among those with increased depressive symptoms. Interventions that focus on emotion regulation might use these electrocortical markers to track changes in regulatory efficacy.     

Revisiting the association between maternal smoking during pregnancy and ADHD

Objective

Studies examining the relationship between maternal smoking during pregnancy and the development of Attention Deficit Hyperactivity Disorder (ADHD) among offspring have yielded mixed results, with some studies suggesting a strong association and others finding no association. These studies have varied in quality of design and measures. The purpose of this study was to evaluate the association between maternal smoking during pregnancy and offspring ADHD, using detailed prospective smoking data and subsequent follow-up data from the Collaborative Perinatal Project (CPP).

Method

Maternal smoking status was collected throughout pregnancy during the original CPP study. Offspring were followed-up in early adulthood and questioned about ADHD symptoms and diagnosis. Logistic regression was used to model the association between maternal smoking during pregnancy and ADHD. Linear and logistic regression were used to examine clinical characteristics and remission rates associated with ADHD in relation to maternal smoking.

Results

No association was found between maternal smoking during pregnancy and offspring ADHD. Further, no differences in age of onset, number of symptoms, or likelihood of remission were found among ADHD subjects with and without a history of maternal smoking during pregnancy.

Conclusions

These findings do not support the hypothesis that maternal smoking during pregnancy is causally related to ADHD. Ongoing research should continue to strive to identify those environmental or genetic factors that may enhance the impact of maternal smoking on ADHD or that may be associated more clearly with the development and potential prevention of ADHD.