Breastfeeding at Any Cost? Adverse Effects of Breastfeeding Pain on Mother-Infant Behavior.

Breast milk is considered the ideal infant nutrition, and medical organizations encourage breastfeeding worldwide. Moreover, breastfeeding is often perceived as a natural and spontaneous socio-biological process and one of the fundamental roles of new mothers. While breastfeeding is beneficial, little scientific consideration has been given to its potential psychological challenges. Here, we investigate the phenomenon of breastfeeding pain in mothers and its association with maternal and infant behavioral regulation. During the postpartum weeks, the mother-infant dyad can be considered one allostatic unit directed at infant regulation and development. We hypothesize that pain comprises an allostatic challenge for mothers and will thus impair the capacity for dyadic regulation. To test this, we recruited 71 mothers with varying levels of breastfeeding pain and videotaped them with their infants (2-35 weeks old) during spontaneous face-to-face interactions. We quantified the individual differences in dyadic regulation by behaviorally coding the second-by-second affective expressions for each mother and infant throughout their interactions. We tested the extent to which breastfeeding pain alters affect regulation during mother-infant interactions. We discovered that mothers with severe breastfeeding pain express less affective expressions and less infant-directed gaze during interactive moments of engagement and play than mothers with no or moderate pain. Moreover, infants of mothers experiencing pain during breastfeeding express less affective expressions and more mother-directed gaze while interacting with their mothers than infants of mothers who are not in pain. This demonstrates that the allostatic challenge of maternal pain interferes with the behavioral regulation of both mothers and infants. Since the mother-infant dyad is a codependent allostatic unit, the allostatic challenges of one partner can impact the dyad and thus potentially impact child development, bonding, and mother and infant well-being. The challenges of breastfeeding should be considered in addition to the nutritional advances.

Evidence for cultural differences in affect during mother-infant interactions.

Maternal care is considered a universal and even cross-species set of typical behaviors, which are necessary to determine the social development of children. In humans, most research on mother-infant bonding is based on Western cultures and conducted in European and American countries. Thus, it is still unknown which aspects of mother-infant behaviors are universal and which vary with culture. Here we test whether typical mother-infant behaviors of affect-communication and affect-regulation are equally represented during spontaneous interaction in Palestinian-Arab and Jewish cultures. 30 Palestinian-Arab and 43 Jewish mother-infant dyads were recruited and videotaped. Using AffectRegulation Coding System (ARCS), we behaviorally analyzed the second-by-second display of valence and arousal in each participant and calculated the dynamic patterns of affect co-regulation. The results show that Palestinian-Arab infants express more positive valence than Jewish infants and that Palestinian-Arab mothers express higher arousal compared to Jewish mothers. Moreover, we found culturally-distinct strategies to regulate the infant: increased arousal in Palestinian-Arab dyads and increased mutual affective match in Jewish dyads. Such cross-cultural differences in affect indicate that basic features of emotion that are often considered universal are differentially represented in different cultures. Affect communication and regulation patterns can be transmitted across generations in early-life socialization with caregivers.

The impact of sociality and affective valence on brain activation: A meta-analysis.

Thirty years of neuroimaging reveal the set of brain regions consistently associated with pleasant and unpleasant affect in humans-or the neural reference space for valence. Yet some of humans' most potent affective states occur in the context of other humans. Prior work has yet to differentiate how the neural reference space for valence varies as a product of the sociality of affective stimuli. To address this question, we meta-analyzed across 614 social and non-social affective neuroimaging contrasts, summarizing the brain regions that are consistently activated for social and non-social affective information. We demonstrate that across the literature, social and non-social affective stimuli yield overlapping activations within regions associated with visceromotor control, including the amygdala, hypothalamus, anterior cingulate cortex and insula. However, we find that social processing differs from non-social affective processing in that it involves additional cortical activations in the medial prefrontal and posterior cingulum that have been associated with mentalizing and prediction. A Bayesian classifier was able to differentiate unpleasant from pleasant affect, but not social from non-social affective states. Moreover, it was not able to classify unpleasantness from pleasantness at the highest levels of sociality. These findings suggest that highly social scenarios may be equally salient to humans, regardless of their valence.

Common model of stress, anxiety, and depressive symptoms in pregnant women from seven high-income Western countries at the COVID-19 pandemic onset.

OBJECTIVE: Increases in stress, anxiety, and depression among women pregnant during the COVID-19 pandemic have been reported internationally. Yet rigorous comparison of the prevalence of maternal mental health problems across countries is lacking. Moreover, whether stress is a common predictor of maternal mental health during the pandemic across countries is unknown. METHODS: 8148 pregnant women from Germany, Israel, Italy, Poland, Spain, Switzerland, and the United States were enrolled in the International COVID-19 Pregnancy Experiences (I-COPE) Study between April 17 and May 31, 2020. Sociodemographic characteristics, pandemic-related stress, pregnancy-specific stress, anxiety, and depression were assessed with well-validated instruments. The magnitude of stress and mood disturbances was compared across countries. A path model predicting clinically significant levels of anxiety and depression from maternal characteristics and stress was tested for all study participants and then examined separately in each country with >200 participants. RESULTS: Countries differed significantly in magnitude of pandemic-related pregnancy stress and pandemic-unrelated pregnancy-specific stress, and in prevalence of clinically significant anxiety and depression levels. A well-fitting common path model for the entire sample indicated that mood and anxiety disturbances were strongly predicted by pandemic-related and pregnancy-specific stress after accounting for maternal characteristics. The model was replicated in individual countries. CONCLUSIONS: Although pregnant women in high-income Western countries experienced different levels of stress resulting from the COVID-19 pandemic, stress is a strong, common predictor of anxiety and depressive symptoms in these individuals. The common model can be used to inform research and clinical interventions to protect against adverse consequences of prenatal maternal stress, anxiety, and depression for mothers and infants.

Bio-behavioral synchrony is a potential mechanism for mate selection in humans.

The decision with whom to form a romantic bond is of great importance, yet the biological or behavioral mechanisms underlying this selective process in humans are largely unknown. Classic evolutionary theories of mate selection emphasize immediate and static features such as physical appearance and fertility. However, they do not explain how initial attraction temporally unfolds during an interaction, nor account for mutual physiological or behavioral adaptations that take place when two people become attracted. Instead, recent theories on social bonding emphasize the importance of co-regulation during social interactions (i.e., the social coordination of physiology and behavior between partners), and predict that co-regulation plays a role in bonding with others. In a speed-date experiment of forty-six heterosexual dates, we recorded the naturally occurring patterns of electrodermal activity and behavioral motion in men and women, and calculated their co-regulation during the date. We demonstrate that co-regulation of behavior and physiology is associated with the date outcome: when a man and a woman synchronize their electrodermal activity and dynamically tune their behavior to one another, they are more likely to be romantically and sexually attracted to one another. This study supports the hypothesis that co-regulation of sympathetic and behavioral rhythms between a man and a woman serves as a mechanism that promotes attraction.

Maternal dopamine encodes affective signals of human infants.

Mothers are highly responsive to their offspring. In non-human mammals, mothers secrete dopamine in the nucleus accumbens (NAcc) in response to their pups. Yet, it is still unknown which aspect of the offspring behavior elicits dopaminergic responses in mothers. Here, we tested whether infants' affective signals elicit dopaminergic responses in the NAcc of human mothers. First, we conducted a behavioral analysis on videos of infants' free play and quantified the affective signals infants spontaneously communicated. Then, we presented the same videos to mothers during a magnetic resonance-positron emission tomography scan. We traced the binding of [11C]raclopride to free D2/3-type receptors to assess maternal dopaminergic responses during the infant videos. When mothers observed videos with many infant signals during the scan, they had less [11C]raclopride binding in the right NAcc. Less [11C]raclopride binding indicates that less D2/3 receptors were free, possibly due to increased endogenous dopamine responses to infants' affective signals. We conclude that NAcc D2/3 receptors are involved in maternal responsiveness to affective signals of human infants. D2/3 receptors have been associated with maternal responsiveness in nonhuman animals. This evidence supports a similar mechanism in humans and specifies infant-behaviors that activate the maternal dopaminergic system, with implications for social neuroscience, development and psychopathology.

What Is Social about Autism? The Role of Allostasis-Driven Learning.

Scientific research on neuro-cognitive mechanisms of autism often focuses on circuits that support social functioning. However, autism is a heterogeneous developmental variation in multiple domains, including social communication, but also language, cognition, and sensory-motor control. This suggests that the underlying mechanisms of autism share a domain-general foundation that impacts all of these processes. In this Perspective Review, we propose that autism is not a social deficit that results from an atypical "social brain". Instead, typical social development relies on learning. In social animals, infants depend on their caregivers for survival, which makes social information vitally salient. The infant must learn to socially interact in order to survive and develop, and the most prominent learning in early life is crafted by social interactions. Therefore, the most prominent outcome of a learning variation is atypical social development. To support the hypothesis that autism results from a variation in learning, we first review evidence from neuroscience and developmental science, demonstrating that typical social development depends on two domain-general processes that determine learning: (a) motivation, guided by allostatic regulation of the internal milieu; and (b) multi-modal associations, determined by the statistical regularities of the external milieu. These two processes are basic ingredients of typical development because they determine allostasis-driven learning of the social environment. We then review evidence showing that allostasis and learning are affected among individuals with autism, both neurally and behaviorally. We conclude by proposing a novel domain-general framework that emphasizes allostasis-driven learning as a key process underlying autism. Guided by allostasis, humans learn to become social, therefore, the atypical social profile seen in autism can reflect a domain-general variation in allostasis-driven learning. This domain-general view raises novel research questions in both basic and clinical research and points to targets for clinical intervention that can lower the age of diagnosis and improve the well-being of individuals with autism.

Musicality was not selected for, rather humans have a good reason to learn music.

We propose that not social bonding, but rather a different mechanism underlies the development of musicality: being unable to survive alone. The evolutionary constraint of being dependent on other humans for survival provides the ultimate driving force for acquiring human faculties such as sociality and musicality, through mechanisms of learning and neural plasticity. This evolutionary mechanism maximizes adaptation to a dynamic environment.

Women's Depressive Symptoms during the COVID-19 Pandemic: The Role of Pregnancy.

The Coronavirus Disease 2019 (COVID-19) pandemic has multiple ramifications for pregnant women. Untreated depression during pregnancy may have long-term effects on the mother and offspring. Therefore, delineating the effects of pregnancy on the mental health of reproductive-age women is crucial. This study aims to determine the risk for depressive symptoms in pregnant and non-pregnant women during COVID-19, and to identify its bio-psycho-social contributors. A total of 1114 pregnant and 256 non-pregnant women were recruited via social media in May 2020 to complete an online survey that included depression and anxiety questionnaires, as well as demographic, obstetric and COVID-19-related questionnaires. Pregnant women also completed the Pandemic-Related Pregnancy Stress Scale (PREPS). Pregnant women reported fewer depressive symptoms and were less concerned that they had COVID-19 than non-pregnant women. Among pregnant women, risk factors for depression included lower income, fewer children, unemployment, thinking that one has COVID-19, high-risk pregnancy, earlier gestational age, and increased pregnancy-related stress. Protective factors included increased partner support, healthy behaviors, and positive appraisal of the pregnancy. Thus, being pregnant is associated with reduced risk for depressive symptoms during the pandemic. Increased social support, engaging in health behaviors and positive appraisal may enhance resilience. Future studies of pregnant versus non-pregnant women could clarify the role of pregnancy during stressful events, and clarify aspects of susceptibility and resilience during pregnancy.

The impact of affective information on working memory: A pair of meta-analytic reviews of behavioral and neuroimaging evidence.

Everyday life is defined by goal states that are continuously reprioritized based on available, often affective information. To pursue these goals, individuals need to process and maintain goal-relevant information, while ignoring potentially salient information that distracts resources from these goals. Empirically, this ability has typically been operationalized as working memory (WM) capacity. A growing body of research is investigating the impact of information's affective salience on WM capacity. In the present review we address this question by exploring the potential differential impact of affective compared with neutral information on WM, and the underlying neural substrates. One-hundred and 65 studies (N = 7,433) were included in the meta-analysis. Results showed negligible to small (d̂ = -.07-.20) effects of affective information on behavioral measures of WM in healthy individuals (n = 4,936) that varied as a function of valence and task-relevance. Heterogeneity analyses were significant, demonstrating the need to identify further study-specific factors and individual differences that moderate affective WM. At the neural level (33 studies; n = 683), processing affective versus neutral material during WM tasks was associated with more frequent recruitment of the vlPFC, the amygdala, and the temporo-occipital cortex. In contrast to healthy individuals, across behavioral studies those suffering from mental health problems (n = 2,041) showed impaired WM accuracy (d̂ = -0.21) in the presence of affective material. These findings highlight the importance of integrating behavioral and neural levels of analysis. Finally, these findings suggest that affective WM capacity may be a transdiagnostic mechanism associated with poor mental health. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Bayesian log-Gaussian Cox process regression: with applications to meta-analysis of neuroimaging working memory studies.

Working memory (WM) was one of the first cognitive processes studied with functional magnetic resonance imaging (fMRI). With now over 20 years of studies on WM, each study with tiny sample sizes, there is a need for meta-analysis to identify the brain regions consistently activated by WM tasks, and to understand the inter-study variation in those activations. However, current methods in the field cannot fully account for the spatial nature of neuroimaging meta-analysis data or the heterogeneity observed among WM studies. In this work, we propose a fully Bayesian random-effects meta-regression model based on log-Gaussian Cox processes, which can be used for meta-analysis of neuroimaging studies. An efficient MCMC scheme for posterior simulations is presented which makes use of some recent advances in parallel computing using graphics processing units (GPUs). Application of the proposed model to a real dataset provides valuable insights regarding the function of the WM.

Growing a social brain.

It has long been assumed that social animals, such as humans, are born with a brain system that has evolved to support social affiliation. However, the evidence does not necessarily support this assumption. Alternatively, social animals can be defined as those who cannot survive alone and rely on members from their group to regulate their ongoing physiology (or allostasis). The rather simple evolutionary constraint of social dependency for survival can be sufficient to make the social environment vitally salient, and to provide the ultimate driving force for socially crafted brain development and learning. In this Perspective, we propose a framework for sociality and specify a set of hypotheses on the mechanisms of social development and underlying neural systems. The theoretical shift proposed here implies that profound human characteristics, including but not limited to sociality, are acquired at an early age, while social interactions provide key wiring instructions that determine brain development.

Author Correction: Growing a social brain.

In the version of this Perspective originally published, at the end of the first paragraph of the section 'Neural prediction as a potential mechanism for how experience sculpts the developing brain' the citation to ref. 76 should have been to ref. 74, and at the end of the first sentence of the next paragraph ref. 76 should have been cited alongside ref. 74. These have now been corrected.

Bio-behavioral synchrony promotes the development of conceptualized emotions.

As adults, we have structured conceptual representations of our emotions that help us to make sense of and regulate our ongoing affective experience. The ability to use emotion concepts is critical to make predictions about the world and choose appropriate action, such as 'I am afraid, and going to run away' or 'I am hungry and going to eat'. Thus, emotion concepts have an important role in helping us maintain our ongoing physiological balance, or allostasis. We will suggest here that infants can learn emotion concepts for the purpose of allostasis regulation, and that conceptualization is key component in emotional development. Moreover, we will suggest that social dyads facilitate concept learning because of a robust evolutionary feature seen in newborns of social species: they cannot survive alone and depend on conspecifics for allostasis regulation. Such social dependency creates a robust driving force for social learning of emotion concepts, and makes the social dyad, which is designed to regulate the infant's allostasis, an optimal medium for concept learning. In line with that, we will review evidence showing that the neural reference space for emotion overlaps with neural circuits that support allostasis (striatum, amygdala, and hypothalamus) and conceptualization (medial prefrontal cortex, posterior cingulate cortex), and that their developmental trajectories are interrelated, and depend on synchronous social care.

Dopamine in the medial amygdala network mediates human bonding.

Research in humans and nonhuman animals indicates that social affiliation, and particularly maternal bonding, depends on reward circuitry. Although numerous mechanistic studies in rodents demonstrated that maternal bonding depends on striatal dopamine transmission, the neurochemistry supporting maternal behavior in humans has not been described so far. In this study, we tested the role of central dopamine in human bonding. We applied a combined functional MRI-PET scanner to simultaneously probe mothers' dopamine responses to their infants and the connectivity between the nucleus accumbens (NAcc), the amygdala, and the medial prefrontal cortex (mPFC), which form an intrinsic network (referred to as the "medial amygdala network") that supports social functioning. We also measured the mothers' behavioral synchrony with their infants and plasma oxytocin. The results of this study suggest that synchronous maternal behavior is associated with increased dopamine responses to the mother's infant and stronger intrinsic connectivity within the medial amygdala network. Moreover, stronger network connectivity is associated with increased dopamine responses within the network and decreased plasma oxytocin. Together, these data indicate that dopamine is involved in human bonding. Compared with other mammals, humans have an unusually complex social life. The complexity of human bonding cannot be fully captured in nonhuman animal models, particularly in pathological bonding, such as that in autistic spectrum disorder or postpartum depression. Thus, investigations of the neurochemistry of social bonding in humans, for which this study provides initial evidence, are warranted.

Functional connectivity dynamics during film viewing reveal common networks for different emotional experiences.

Recent theoretical and empirical work has highlighted the role of domain-general, large-scale brain networks in generating emotional experiences. These networks are hypothesized to process aspects of emotional experiences that are not unique to a specific emotional category (e.g., "sadness," "happiness"), but rather that generalize across categories. In this article, we examined the dynamic interactions (i.e., changing cohesiveness) between specific domain-general networks across time while participants experienced various instances of sadness, fear, and anger. We used a novel method for probing the network connectivity dynamics between two salience networks and three amygdala-based networks. We hypothesized, and found, that the functional connectivity between these networks covaried with the intensity of different emotional experiences. Stronger connectivity between the dorsal salience network and the medial amygdala network was associated with more intense ratings of emotional experience across six different instances of the three emotion categories examined. Also, stronger connectivity between the dorsal salience network and the ventrolateral amygdala network was associated with more intense ratings of emotional experience across five out of the six different instances. Our findings demonstrate that a variety of emotional experiences are associated with dynamic interactions of domain-general neural systems.

The brain basis of social synchrony.

As a social species, humans evolved to detect information from the social behavior of others. Yet, the mechanisms used to evaluate social interactions, the brain networks implicated in such recognition, and whether individual differences in own social behavior determine response to similar behavior in others remain unknown. Here we examined social synchrony as a potentially important mechanism in the evaluation of social behavior and utilized the parenting context, an evolutionarily salient setting of significant consequences for infant survival, to test this issue. The brain response of healthy postpartum mothers to three mother-infant interaction vignettes was assessed. Videos included a typical synchronous interaction and two pathological interactions of mothers diagnosed with postpartum depression and anxiety that showed marked deviations from social synchrony. Mothers' own interactions with their 4- to 6-month-old infants were videotaped and micro-coded for synchrony. Results indicated that the recognition of social synchrony involved activations in the dorsal anterior cingulate cortex (dACC), fusiform, cuneus, inferior parietal lobule, supplementary motor area and NAcc. Mother's own synchrony with her infant correlated with her dACC response to synchrony in others. Findings are consistent with models suggesting that social action underpins social recognition and highlight social synchrony and the mother-infant bond as one prototypical context for studying the brain basis of social understanding.

Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin.

OBJECTIVE: Research on the neurobiology of parenting has defined biobehavioral synchrony, the coordination of biological and behavioral responses between parent and child, as a central process underpinning mammalian bond formation. Bi-parental rearing, typically observed in monogamous species, is similarly thought to draw on mechanisms of mother-father synchrony. METHOD: We examined synchrony in mothers' and fathers' brain response to ecologically valid infant cues. Thirty mothers and fathers, comprising 15 couples parenting 4- to 6-month-old infants, were visited at home, and infant play was videotaped. Parents then underwent functional magnetic resonance imaging scanning while observing own-infant compared with standard-infant videos. Coordination in brain response between mothers and fathers was assessed using a voxel-by-voxel algorithm, and gender-specific activations were also tested. Plasma oxytocin and arginine vasopressin, neuropeptides implicated in female and male bonding, were examined as correlates. RESULTS: Online coordination in maternal and paternal brain activations emerged in social-cognitive networks implicated in empathy and social cognition. Mothers showed higher amygdala activations and correlations between amygdala response and oxytocin. Fathers showed greater activations in social-cognitive circuits, which correlated with vasopressin. CONCLUSIONS: Parents coordinate online activity in social-cognitive networks that support intuitive understanding of infant signals and planning of adequate caregiving, whereas motivational-limbic activations may be gender specific. Although preliminary, these findings demonstrate synchrony in the brain response of two individuals within an attachment relationship, and may suggest that human attachment develops within the matrix of biological attunement and brain-to-brain synchrony between attachment partners.

Specifying the neurobiological basis of human attachment: brain, hormones, and behavior in synchronous and intrusive mothers.

The mother-infant bond provides the foundation for the infant's future mental health and adaptation and depends on the provision of species-typical maternal behaviors that are supported by neuroendocrine and motivation-affective neural systems. Animal research has demonstrated that natural variations in patterns of maternal care chart discrete profiles of maternal brain-behavior relationships that uniquely shape the infant's lifetime capacities for stress regulation and social affiliation. Such patterns of maternal care are mediated by the neuropeptide Oxytocin and by stress- and reward-related neural systems. Human studies have similarly shown that maternal synchrony--the coordination of maternal behavior with infant signals--and intrusiveness--the excessive expression of maternal behavior--describe distinct and stable maternal styles that bear long-term consequences for infant well-being. To integrate brain, hormones, and behavior in the study of maternal-infant bonding, we examined the fMRI responses of synchronous vs intrusive mothers to dynamic, ecologically valid infant videos and their correlations with plasma Oxytocin. In all, 23 mothers were videotaped at home interacting with their infants and plasma OT assayed. Sessions were micro-coded for synchrony and intrusiveness. Mothers were scanned while observing several own and standard infant-related vignettes. Synchronous mothers showed greater activations in the left nucleus accumbens (NAcc) and intrusive mothers exhibited higher activations in the right amygdala. Functional connectivity analysis revealed that among synchronous mothers, left NAcc and right amygdala were functionally correlated with emotion modulation, theory-of-mind, and empathy networks. Among intrusive mothers, left NAcc and right amygdala were functionally correlated with pro-action areas. Sorting points into neighborhood (SPIN) analysis demonstrated that in the synchronous group, left NAcc and right amygdala activations showed clearer organization across time, whereas among intrusive mothers, activations of these nuclei exhibited greater cross-time disorganization. Correlations between Oxytocin with left NAcc and right amygdala activations were found only in the synchronous group. Well-adapted parenting appears to be underlay by reward-related motivational mechanisms, temporal organization, and affiliation hormones, whereas anxious parenting is likely mediated by stress-related mechanisms and greater neural disorganization. Assessing the integration of motivation and social networks into unified neural activity that reflects variations in patterns of parental care may prove useful for the study of optimal vs high-risk parenting.

Immune perturbations in patients along the perioperative period: alterations in cell surface markers and leukocyte subtypes before and after surgery.

BACKGROUND: Surgery renders patients susceptible to life-threatening complications, including infections, multiple organ failure, and presumably cancer metastases. Surgery-induced immune perturbations were suggested to contribute to such deleterious effects, but also to facilitate post-injury healing. Preoperative psychological and physiological stress responses may contribute to these immune perturbations, and could thus jeopardize patients even before surgery. The current study assessed the effects of various operations on an array of immune indices during the perioperative period. To qualify immune changes before surgery, patients' immune status was also compared to that of healthy controls. METHODS: A total of 81 subjects (operated patients and healthy controls) provided up to five daily blood samples during the perioperative period, for assessment of leukocyte subtypes (granulocytes, monocytes, Tc, Th, NK, NKT, CD4+CD25+, CD8(bright)CD4(dim), and B cells) and their surface markers (HLA-DR and LFA-1). RESULTS: Even before surgery patients displayed immune perturbations, including reduced lymphocyte HLA-DR expression and increased monocyte LFA-1 expression. Following surgery, we recorded a reduction in lymphocyte numbers that was subtype specific, increased granulocyte numbers, and reduced expression of HLA-DR by lymphocytes and monocytes. Finally, no significant associations were found between alteration in leukocyte numbers and cell surface markers (although these indices showed high correlations with other variables), implying differential mediating mechanisms. CONCLUSION: Several immune alterations are manifested prior to surgery, and contribute to the marked postoperative changes, which are commonly interpreted as immune suppression. We discuss the possible adaptive and maladaptive nature of these perturbations in the context of natural injury, stress, and surgery.