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.     

When you smile,the world smiles at you: ERP evidence for self-expression effects on face processing

Current models of emotion simulation propose that intentionally posing a facial expression can change one’s subjective feelings, which in turn influences the processing of visual input. However, the underlying neural mechanism whereby one’s facial emotion modulates the visual cortical responses to other’s facial expressions remains unknown. To understand how one’s facial expression affects visual processing, we measured participants’ visual evoked potentials (VEPs) during a facial emotion judgment task of positive and neutral faces. To control for the effects of facial muscles on VEPs, we asked participants to smile (adopting an expression of happiness), to purse their lips (incompatible with smiling) or to pose with a neutral face, in separate blocks. Results showed that the smiling expression modulates face-specific visual processing components (N170/vertex positive potential) to watching other facial expressions. Specifically, when making a happy expression, neutral faces are processed similarly to happy faces. When making a neutral expression or pursing the lips, however, responses to neutral and happy face are significantly different. This effect was source localized within multisensory associative areas, angular gyrus, associative visual cortex and somatosensory cortex. We provide novel evidence that one’s own emotional expression acts as a top-down influence modulating low-level neural encoding during facial perception.     

Eye contact influences neural processing of emotional expressions in 4-month-old infants

Eye gaze is a fundamental component of human communication.During the first post-natal year, infants rapidly learn thatthe gaze of others provides socially significant information.In addition, infants are sensitive to several emotional expressions.However, little is known regarding how eye contact influencesthe way the infant brain processes emotional expressions. Wemeasured 4-month-old infants’ brain electric activityto assess neural processing of faces displaying neutral, happyand angry emotional expressions when accompanied by direct andaverted eye gaze. The results show that processing of angryfacial expressions was influenced by eye gaze. In particular,infants showed enhanced neural processing of angry expressionswhen these expressions were accompanied by direct eye gaze.These results show that by 4 months of age, the infant detectsangry emotional expressions, and the infant brain processestheir relevance to the self.     

A cry in the dark: depressed mothers show reduced neural activation to their own infant's cry

This study investigated depression-related differences in primiparous mothers’ neural response to their own infant’s distress cues. Mothers diagnosed with major depressive disorder (n = 11) and comparison mothers with no diagnosable psychopathology (n = 11) were exposed to their own 18-months-old infant’s cry sound, as well as unfamiliar infant’s cry and control sound, during functional neuroimaging. Depressed mothers’ response to own infant cry greater than other sounds was compared to non-depressed mothers’ response in the whole brain [false discovery rate (FDR) corrected]. A continuous measure of self-reported depressive symptoms (CESD) was also tested as a predictor of maternal response. Non-depressed mothers activated to their own infant’s cry greater than control sound in a distributed network of para/limbic and prefrontal regions, whereas depressed mothers as a group failed to show activation. Non-depressed compared to depressed mothers showed significantly greater striatal (caudate, nucleus accumbens) and medial thalamic activation. Additionally, mothers with lower depressive symptoms activated more strongly in left orbitofrontal, dorsal anterior cingulate and medial superior frontal regions. Non-depressed compared to depressed mothers activated uniquely to own infant greater than other infant cry in occipital fusiform areas. Disturbance of these neural networks involved in emotional response and regulation may help to explain parenting deficits in depressed mothers.     

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.     

Emotion unfolded by motion: a role for parietal lobe in decoding dynamic facial expressions

Facial expressions convey important emotional and social information and are frequently applied in investigations of human affective processing. Dynamic faces may provide higher ecological validity to examine perceptual and cognitive processing of facial expressions. Higher order processing of emotional faces was addressed by varying the task and virtual face models systematically. Blood oxygenation level-dependent activation was assessed using functional magnetic resonance imaging in 20 healthy volunteers while viewing and evaluating either emotion or gender intensity of dynamic face stimuli. A general linear model analysis revealed that high valence activated a network of motion-responsive areas, indicating that visual motion areas support perceptual coding for the motion-based intensity of facial expressions. The comparison of emotion with gender discrimination task revealed increased activation of inferior parietal lobule, which highlights the involvement of parietal areas in processing of high level features of faces. Dynamic emotional stimuli may help to emphasize functions of the hypothesized ‘extended’ over the ‘core’ system for face processing.     

The impact of depression on mothers’ neural processing of their adolescents’ affective behavior

Depression affects neural processing of emotional stimuli and could, therefore, impact parent–child interactions. However, the neural processes with which mothers with depression process their adolescents’ affective interpersonal signals and how this relates to mothers’ parenting behavior are poorly understood. Mothers with and without depression (N = 64 and N = 51, respectively; M_age = 40 years) from low-income families completed an interaction task with their adolescents (M_age = 12.8 years), which was coded for both individuals’ aggressive, dysphoric, positive and neutral affective behavior. While undergoing fMRI, mothers viewed video clips from this task of affective behavior from their own and an unfamiliar adolescent. Relative to non-depressed mothers, those with depression showed more aggressive and less positive affective behavior during the interaction task and more activation in the bilateral insula, superior temporal gyrus and striatum but less in the lateral prefrontal cortex while viewing aggressive and neutral affect. Findings were comparable for own and unfamiliar adolescents’ affect. Heightened limbic, striatal and sensory responses were associated with more aggressive and dysphoric parenting behavior during the interactions, while reduced lateral prefrontal activation was associated with less positive parenting behavior. These results highlight the importance of depressed mothers’ affective information processing for understanding mothers’ behavior during interactions with their adolescents.     

Oxytocin enhances pupil dilation and sensitivity to ‘hidden’ emotional expressions

Sensing others’ emotions through subtle facial expressions is a highly important social skill. We investigated the effects of intranasal oxytocin treatment on the evaluation of explicit and ‘hidden’ emotional expressions and related the results to individual differences in sensitivity to others’ subtle expressions of anger and happiness. Forty healthy volunteers participated in this double-blind, placebo-controlled crossover study, which shows that a single dose of intranasal oxytocin (40 IU) enhanced or ‘sharpened’ evaluative processing of others’ positive and negative facial expression for both explicit and hidden emotional information. Our results point to mechanisms that could underpin oxytocin’s prosocial effects in humans. Importantly, individual differences in baseline emotional sensitivity predicted oxytocin’s effects on the ability to sense differences between faces with hidden emotional information. Participants with low emotional sensitivity showed greater oxytocin-induced improvement. These participants also showed larger task-related pupil dilation, suggesting that they also allocated the most attentional resources to the task. Overall, oxytocin treatment enhanced stimulus-induced pupil dilation, consistent with oxytocin enhancement of attention towards socially relevant stimuli. Since pupil dilation can be associated with increased attractiveness and approach behaviour, this effect could also represent a mechanism by which oxytocin increases human affiliation.     

Categorization and evaluation of emotional faces in psychopathic women

Psychopathic individuals have been shown to respond less strongly than normal controls to emotional stimuli. Data about their ability to judge emotional facial expressions are inconsistent and limited to males. To measure categorical and dimensional evaluations of emotional facial expressions in psychopathic and non-psychopathic women, 13 female psychopathic forensic inpatients, 15 female non-psychopathic forensic inmates and 16 female healthy participants were tested in an emotion-categorizing task. Emotional facial expressions were presented briefly (33 ms) or until buttonpress. Participants were to classify emotional expressions, and to rate their valence and arousal. Group differences in categorization were observed at both presentation times. Psychopathic patients performed worst with briefly presented sad expressions. Moreover, their dimensional evaluation resulted in less positive ratings for happy expressions and less arousal for angry expressions compared with the responses of non-psychopathic and normal subjects. Results shed light on the mechanism possibly underlying the emotional deficits in psychopathic women.     

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.     

Affective resonance in response to others’ emotional faces varies with affective ratings and psychopathic traits in amygdala and anterior insula

Despite extensive research on the neural basis of empathic responses for pain and disgust, there is limited data about the brain regions that underpin affective response to other people’s emotional facial expressions. Here, we addressed this question using event-related functional magnetic resonance imaging to assess neural responses to emotional faces, combined with online ratings of subjective state. When instructed to rate their own affective response to others’ faces, participants recruited anterior insula, dorsal anterior cingulate, inferior frontal gyrus, and amygdala, regions consistently implicated in studies investigating empathy for disgust and pain, as well as emotional saliency. Importantly, responses in anterior insula and amygdala were modulated by trial-by-trial variations in subjective affective responses to the emotional facial stimuli. Furthermore, overall task-elicited activations in these regions were negatively associated with psychopathic personality traits, which are characterized by low affective empathy. Our findings suggest that anterior insula and amygdala play important roles in the generation of affective internal states in response to others’ emotional cues and that attenuated function in these regions may underlie reduced empathy in individuals with high levels of psychopathic traits.     

Hormonal contraceptives,menstrual cycle and brain response to faces

Both behavioral and neuroimaging evidence support a female advantage in the perception of human faces. Here we explored the possibility that this relationship may be partially mediated by female sex hormones by investigating the relationship between the brain’s response to faces and the use of oral contraceptives, as well as the phase of the menstrual cycle. First, functional magnetic resonance images were acquired in 20 young women [10 freely cycling and 10 taking oral contraception (OC)] during two phases of their cycle: mid-cycle and menstruation. We found stronger neural responses to faces in the right fusiform face area (FFA) in women taking oral contraceptives (vs freely cycling women) and during mid-cycle (vs menstruation) in both groups. Mean blood oxygenation level-dependent response in both left and right FFA increased as function of the duration of OC use. Next, this relationship between the use of OC and FFA response was replicated in an independent sample of 110 adolescent girls. Finally in a parallel behavioral study carried out in another sample of women, we found no evidence of differences in the pattern of eye movements while viewing faces between freely cycling women vs those taking oral contraceptives. The imaging findings might indicate enhanced processing of social cues in women taking OC and women during mid-cycle.     

Subcortical BOLD responses during visual sexual stimulation vary as a function of implicit porn associations in women

Lifetime experiences shape people’s attitudes toward sexual stimuli. Visual sexual stimulation (VSS), for instance, may be perceived as pleasurable by some, but as disgusting or ambiguous by others. VSS depicting explicit penile–vaginal penetration (PEN) is relevant in this respect, because the act of penetration is a core sexual activity. In this study, 20 women without sexual complaints participated. We used functional magnetic resonance imaging and a single-target implicit association task to investigate how brain responses to PEN were modulated by the initial associations in memory (PEN-‘hot’ vs PEN-disgust) with such hardcore pornographic stimuli. Many brain areas responded to PEN in the same way they responded to disgust stimuli, and PEN-induced brain activity was prone to modulation by subjective disgust ratings toward PEN stimuli. The relative implicit PEN-disgust (relative to PEN-‘hot’) associations exclusively modulated PEN-induced brain responses: comparatively negative (PEN-disgust) implicit associations with pornography predicted the strongest PEN-related responses in the basal forebrain (including nucleus accumbens and bed nucleus of stria terminalis), midbrain and amygdala. Since these areas are often implicated in visual sexual processing, the present findings should be taken as a warning: apparently their involvement may also indicate a negative or ambivalent attitude toward sexual stimuli.     

Processing of facial expressions of same-race and other-race faces: distinct and shared neural underpinnings

People understand others’ emotions quickly from their facial expressions. However, facial expressions of ingroup and outgroup members may signal different social information and thus be mediated by distinct neural activities. We investigated whether there are distinct neuronal responses to fearful and happy expressions of same-race (SR) and other-race (OR) faces. We recorded electroencephalogram from Chinese adults when viewing an adaptor face (with fearful/neutral expressions in Experiment 1 but happy/neutral expressions in Experiment 2) and a target face (with fearful expressions in Experiment 1 but happy expressions in Experiment 2) presented in rapid succession. We found that both fearful and happy (vs neutral) adaptor faces increased the amplitude of a frontocentral positivity (P2). However, a fearful but not happy (vs neutral) adaptor face decreased the P2 amplitudes to target faces, and this repetition suppression (RS) effect occurred when adaptor and target faces were of the same race but not when of different races. RS was observed on two late parietal/central positive activities to fearful/happy target faces, which, however, occurred regardless of whether adaptor and target faces were of the same or different races. Our findings suggest that early affective processing of fearful expressions may engage distinct neural activities for SR and OR faces.     

‘Ecstasy’ as a social drug: MDMA preferentially affects responses to emotional stimuli with social content

3,4-Methylenedioxymethamphetamine (MDMA, ‘ecstasy’) is used recreationally to improve mood and sociability, and has generated clinical interest as a possible adjunct to psychotherapy. One way that MDMA may produce positive ‘prosocial’ effects is by changing responses to emotional stimuli, especially stimuli with social content. Here, we examined for the first time how MDMA affects subjective responses to positive, negative and neutral emotional pictures with and without social content. We hypothesized that MDMA would dose-dependently increase reactivity to positive emotional stimuli and dampen reactivity to negative stimuli, and that these effects would be most pronounced for pictures with people in them. The data were obtained from two studies using similar designs with healthy occasional MDMA users (total N = 101). During each session, participants received MDMA (0, 0.75 and 1.5 mg/kg oral), and then rated their positive and negative responses to standardized positive, negative and neutral pictures with and without social content. MDMA increased positive ratings of positive social pictures, but reduced positive ratings of non-social positive pictures. We speculate this ‘socially selective’ effect contributes to the prosocial effects of MDMA by increasing the comparative value of social contact and closeness with others. This effect may also contribute to its attractiveness to recreational users.     

Heterogeneity in brain reactivity to pleasant and food cues: evidence of sign-tracking in humans

Aberrant brain reward responses to food-related cues are an implied characteristic of human obesity; yet, findings are inconsistent. To explain these inconsistencies, we aimed to uncover endophenotypes associated with heterogeneity in attributing incentive salience to food cues in the context of other emotionally salient cues; a phenomenon described as sign- vs goal tracking in preclinical models. Data from 64 lean and 88 obese adults who were 35.5 ± 9.4 years old and predominantly women (79%) were analyzed. Participants viewed food-related, pleasant, neutral and unpleasant images while recording electroencephalograph. Late positive potentials were used to assess incentive salience attributed to the visual stimuli. Eating and affective traits were also assessed. Findings demonstrated that obese individuals, in general, do not demonstrate aberrant brain reward responses to food-related cues. As hypothesized, latent profile analysis of the late positive potential uncovered two distinct groups. ‘Sign-trackers’ showed greater responses to food-related cues (P < 0.001) but lower responses to pleasant stimuli (P < 0.001) compared with ‘goal-trackers’. There were proportionally more obese than lean ‘sign-trackers’ (P = 0.03). Obese ‘sign-trackers’ reported significantly higher levels of emotional eating and food craving (P < 0.001). By examining the heterogeneity in brain reactivity to various emotional stimuli, this translational study highlights the need to consider important neurobehavioral endophenotypes of obesity.     

Mothers’ pupillary responses to infant facial expressions

Background

Human parental care relies heavily on the ability to monitor and respond to a child’s affective states. The current study examined pupil diameter as a potential physiological index of mothers’ affective response to infant facial expressions.

Methods

Pupillary time-series were measured from 86 mothers of young infants in response to an array of photographic infant faces falling into four emotive categories based on valence (positive vs. negative) and arousal (mild vs. strong).

Results

Pupil dilation was highly sensitive to the valence of facial expressions, being larger for negative vs. positive facial expressions. A separate control experiment with luminance-matched non-face stimuli indicated that the valence effect was specific to facial expressions and cannot be explained by luminance confounds. Pupil response was not sensitive to the arousal level of facial expressions.

Conclusions

The results show the feasibility of using pupil diameter as a marker of mothers’ affective responses to ecologically valid infant stimuli and point to a particularly prompt maternal response to infant distress cues.

     

Mothers’ unresolved trauma blunts amygdala response to infant distress

While the neurobiology of post-traumatic stress disorder has been extensively researched, much less attention has been paid to the neural mechanisms underlying more covert but pervasive types of trauma (e.g., those involving disrupted relationships and insecure attachment). Here, we report on a neurobiological study documenting that mothers’ attachment-related trauma, when unresolved, undermines her optimal brain response to her infant’s distress. We examined the amygdala blood oxygenation level-dependent response in 42 first-time mothers as they underwent functional magnetic resonance imaging scanning, viewing happy- and sad-face images of their own infant, along with those of a matched unknown infant. Whereas mothers with no trauma demonstrated greater amygdala responses to the sad faces of their own infant as compared to their happy faces, mothers who were classified as having unresolved trauma in the Adult Attachment Interview (Dynamic Maturational Model) displayed blunted amygdala responses when cued by their own infants’ sadness as compared to happiness. Unknown infant faces did not elicit differential amygdala responses between the mother groups. The blunting of the amygdala response in traumatized mothers is discussed as a neural indication of mothers’ possible disengagement from infant distress, which may be part of a process linking maternal unresolved trauma and disrupted maternal caregiving.     

An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play

This study tested whether mothers with interpersonal violence-related posttraumatic stress disorder (IPV-PTSD) vs healthy controls (HC) would show greater limbic and less frontocortical activity when viewing young children during separation compared to quiet play. Mothers of 20 children (12–42 months) participated: 11 IPV-PTSD mothers and 9 HC with no PTSD. During fMRI, mothers watched epochs of play and separation from their own and unfamiliar children. The study focused on comparison of PTSD mothers vs HC viewing children in separation vs play, and viewing own vs unfamiliar children in separation. Both groups showed distinct patterns of brain activation in response to viewing children in separation vs play. PTSD mothers showed greater limbic and less frontocortical activity (BA10) than HC. PTSD mothers also reported feeling more stressed than HC when watching own and unfamiliar children during separation. Their self-reported stress was associated with greater limbic and less frontocortical activity. Both groups also showed distinct patterns of brain activation in response to viewing their own vs unfamiliar children during separation. PTSD mothers’ may not have access to frontocortical regulation of limbic response upon seeing own and unfamiliar children in separation. This converges with previously reported associations of maternal IPV-PTSD and atypical caregiving behavior following separation.     

Decoding facial expressions based on face‐selective and motion‐sensitive areas

Humans can easily recognize others' facial expressions. Among the brain substrates that enable this ability, considerable attention has been paid to face‐selective areas; in contrast, whether motion‐sensitive areas, which clearly exhibit sensitivity to facial movements, are involved in facial expression recognition remained unclear. The present functional magnetic resonance imaging (fMRI) study used multi‐voxel pattern analysis (MVPA) to explore facial expression decoding in both face‐selective and motion‐sensitive areas. In a block design experiment, participants viewed facial expressions of six basic emotions (anger, disgust, fear, joy, sadness, and surprise) in images, videos, and eyes‐obscured videos. Due to the use of multiple stimulus types, the impacts of facial motion and eye‐related information on facial expression decoding were also examined. It was found that motion‐sensitive areas showed significant responses to emotional expressions and that dynamic expressions could be successfully decoded in both face‐selective and motion‐sensitive areas. Compared with static stimuli, dynamic expressions elicited consistently higher neural responses and decoding performance in all regions. A significant decrease in both activation and decoding accuracy due to the absence of eye‐related information was also observed. Overall, the findings showed that emotional expressions are represented in motion‐sensitive areas in addition to conventional face‐selective areas, suggesting that motion‐sensitive regions may also effectively contribute to facial expression recognition. The results also suggested that facial motion and eye‐related information played important roles by carrying considerable expression information that could facilitate facial expression recognition. Hum Brain Mapp 38:3113–3125, 2017. © 2017 Wiley Periodicals, Inc.