Mechanisms supporting the social regulation of neural threat responding with marital partners: A test of the opioid hypothesis.

Positive social contact predicts better health, but the mechanisms for this association remain debated. One way to explore this link is through the social regulation of emotion, particularly anticipatory anxiety. Previous research finds less neural threat response during partner handholding than when people are alone or stranger handholding. Various mechanistic accounts have been forwarded, including the hypothesis that this effect is mediated by endogenous opioid activity. This experiment critically tested the opioid hypothesis in 60 married participants and their partners. The study used a naltrexone opioid blockade in a double-blind placebo control with functional magnetic resonance imaging to determine whether endogenous opioids were necessary for handholding effects. Regulatory effects of supportive handholding manifested in threat network regions during opioid blockade, but not with placebo. Despite a surprising lack of effect in the placebo group, the overall study findings provide initial evidence that endogenous opioids may not be necessary for the social regulation of neural threat responding.

Social baseline theory: State of the science and new directions.

Social baseline theory (SBT) maintains that the primary human ecology is a social ecology. Because of this fact, the theory predicts that humans will find it easier and less energetically taxing to regulate emotion and act when in proximity to familiar and predictable others. This article reviews new empirical and theoretical work related to SBT and highlights areas of needed research. Among these exciting developments are investigations of the neural mechanisms of social emotion regulation, the creation of a model of social allostasis, and work investigating at the impact of social proximity in real-world contexts. SBT continues to accrue support and inspire new theoretical and empirical contributions.

The social regulation of emotion: Inconsistencies suggest no mediation through ventromedial prefrontal cortex.

Physical touch in the form of holding a loved one's hand attenuates the neural response to threat. Speculation regarding the neural mediation of this effect points to the ventromedial prefrontal cortex (vmPFC), which is known to have inhibitory connections with threat responsive brain regions such as the amygdala. Despite the attractiveness of this hypothesis, a link between the vmPFC and diminished threat during handholding has been difficult to demonstrate empirically. Here we report that in a sample of 110 participants no evidence for vmPFC mediation of the handholding effect was obtained. Indeed, results indicated that connectivity patterns between threat responsive salience network structures and the vmPFC were in the opposite direction one would predict if the vmPFC mediated reductions in neural threat-responding caused by partner handholding. Our findings suggest that the vmPFC does not mediate the regulating effect of physical contact on neural threat responses.

Manipulation of Self-Expansion Alters Responses to Attractive Alternative Partners.

Past behavioral research has examined relationship infidelity as a potential outcome of focusing on attractive alternative partners when already in a relationship. The extent to which individuals find such alternatives attractive has been shown to be associated with various factors in the relationship, including self-expansion. However, no previous research has tested the role of self-expansion experimentally. This paper presents two experiments that directly manipulate self-expansion to determine the effect of self-expansion on responses to attractive alternative partners. Participants primed to experience a higher need for self-expansion had better memory for attractive alternatives with self-expanding traits dissimilar to their partner's versus attractive alternatives with self-expanding traits similar to their partner's. Additionally, participants primed with self-expansion (via a video of their partner discussing ways in which life with one another is exciting, novel, and challenging), had less fMRI BOLD response to attractive alternatives of the opposite sex in regions associated with perception of attractive faces (anterior cingulate and medial prefrontal cortex) relative to when they were primed with love (via a video of their partner discussing times they felt strong feelings of love for one another), or neutral content (via a video of their partner discussing some times in which they engage in mundane, routine activities together). The magnitude of this effect in the ACC correlated with relationship closeness as measured by the inclusion of the other in the self scale.

Social Allostasis and Social Allostatic Load: A New Model for Research in Social Dynamics, Stress, and Health.

Theories such as social baseline theory have argued that social groups serve a regulatory function but have not explored whether this regulatory process carries costs for the group. Allostatic load, the wear and tear on regulatory systems caused by chronic or frequent stress, is marked by diminished stress system flexibility and compromised recovery. We argue that allostatic load may develop within social groups as well and provide a model for how relationship dysfunction operates. Social allostatic load may be characterized by processes such as groups becoming locked into static patterns of interaction and may ultimately lead to up-regulation or down-regulation of a group's set point, or the optimal range of arousal or affect around which the group tends to converge. Many studies of emotional and physiological linkage within groups have reported that highly correlated states of arousal, which may reflect failure to maintain a group-level regulatory baseline, occur in the context of stress, conflict, and relationship distress. Relationship strain may also place greater demands on neurocognitive regulatory processes. Just as allostatic load may be detrimental to individual health, social allostatic load may corrode relationship quality.

Relationship status and perceived support in the social regulation of neural responses to threat.

Strong social ties correspond with better health and well being, but the neural mechanisms linking social contact to health remain speculative. This study extends work on the social regulation of brain activity by supportive handholding in 110 participants (51 female) of diverse racial and socioeconomic origins. In addition to main effects of social regulation by handholding, we assessed the moderating effects of both perceived social support and relationship status (married, cohabiting, dating or platonic friends). Results suggest that, under threat of shock, handholding by familiar relational partners attenuates both subjective distress and activity in a network associated with salience, vigilance and regulatory self-control. Moreover, greater perceived social support corresponded with less brain activity in an extended network associated with similar processes, but only during partner handholding. In contrast, we did not observe any regulatory effects of handholding by strangers, and relationship status did not moderate the regulatory effects of partner handholding. These findings suggest that contact with a familiar relational partner is likely to attenuate subjective distress and a variety of neural responses associated with the presence of threat. This effect is likely enhanced by an individual's expectation of the availability of support from their wider social network.

Subjective General Health and the Social Regulation of Hypothalamic Activity.

OBJECTIVE: Social support is associated with better health. This association may be partly mediated through the social regulation of adrenomedullary activity related to poor cardiovascular health and glucocorticoid activity known to inhibit immune functioning. These physiological cascades originate in the hypothalamic areas that are involved in the neural response to threat. The aim of the study investigated whether the down regulation, by social support, of hypothalamic responses to threat is associated with better subjective health. METHODS: A diverse community sample of seventy-five individuals, aged 23 to 26 years, were recruited from an ongoing longitudinal study. Participants completed the Short Form Health Survey, a well-validated self-report measure used to assess subjective general health. They were scanned, using functional magnetic resonance imaging, during a threat of shock paradigm involving various levels of social support, which was manipulated using handholding from a close relational partner, a stranger, and an alone condition. We focused on a hypothalamic region of interest derived from an independent sample to examine the association between hypothalamic activity and subjective general health. RESULTS: Results revealed a significant interaction between handholding condition and self-reported general health (F(2,72) = 3.53, p = .032, partial η = 0.05). Down regulation of the hypothalamic region of interest during partner handholding corresponded with higher self-ratings of general health (ß = -0.31, p = .007). CONCLUSIONS: Higher self-ratings of general health correspond with decreased hypothalamic activity during a task that blends threat with supportive handholding. These results suggest that associations between social support and health are partly mediated through the social regulation of hypothalamic sensitivity to threat.

Toward a radically embodied neuroscience of attachment and relationships.

Attachment theory (Bowlby, 1969/1982) posits the existence of internal working models as a foundational feature of human bonds. Radical embodied approaches instead suggest that cognition requires no computation or representation, favoring a cognition situated in a body in an environmental context with affordances for action (Chemero, 2009; Barrett, 2011; Wilson and Golonka, 2013; Casasanto and Lupyan, 2015). We explore whether embodied approaches to social soothing, interpersonal warmth, separation distress, and support seeking could replace representational constructs such as internal working models with a view of relationship cognition anchored in the resources afforded to the individual by their brain, body, and environment in interaction. We review the neurobiological bases for social attachments and relationships and attempt to delineate how these systems overlap or don't with more basic physiological systems in ways that support or contradict a radical embodied explanation. We suggest that many effects might be the result of the fact that relationship cognition depends on and emerges out of the action of neural systems that regulate several clearly physically grounded systems. For example, the neuropeptide oxytocin appears to be central to attachment and pair-bond behavior (Carter and Keverne, 2002) and is implicated in social thermoregulation more broadly, being necessary for maintaining a warm body temperature (for a review, see IJzerman et al., 2015b). Finally, we discuss the most challenging issues around taking a radically embodied perspective on social relationships. We find the most crucial challenge in individual differences in support seeking and responses to social contact, which have long been thought to be a function of representational structures in the mind (e.g., Baldwin, 1995). Together we entertain the thought to explain such individual differences without mediating representations or computations, but in the end propose a hybrid model of radical embodiment and internal representations.

Adolescent neighborhood quality predicts adult dACC response to social exclusion.

Neuroimaging studies using the social-exclusion paradigm Cyberball indicate increased dorsal anterior cingulate cortex (dACC) and right insula activity as a function of exclusion. However, comparatively less work has been done on how social status factors may moderate this finding. This study used the Cyberball paradigm with 85 (45 females) socio-economically diverse participants from a larger longitudinal sample. We tested whether neighborhood quality during adolescence would predict subsequent neural responding to social exclusion in young adulthood. Given previous behavioral studies indicating greater social vigilance and negative evaluation as a function of lower status, we expected that lower adolescent neighborhood quality would predict greater dACC activity during exclusion at young adulthood. Our findings indicate that young adults who lived in low-quality neighborhoods in adolescence showed greater dACC activity to social exclusion than those who lived in higher quality neighborhoods. Lower neighborhood quality also predicted greater prefrontal activation in the superior frontal gyrus, dorsal medial prefrontal cortex and the middle frontal gyrus, possibly indicating greater regulatory effort. Finally, this effect was not driven by subsequent ratings of distress during exclusion. In sum, adolescent neighborhood quality appears to potentiate neural responses to social exclusion in young adulthood, effects that are independent of felt distress.

Soothing the threatened brain: leveraging contact comfort with emotionally focused therapy.

Social relationships are tightly linked to health and well-being. Recent work suggests that social relationships can even serve vital emotion regulation functions by minimizing threat-related neural activity. But relationship distress remains a significant public health problem in North America and elsewhere. A promising approach to helping couples both resolve relationship distress and nurture effective interpersonal functioning is Emotionally Focused Therapy for couples (EFT), a manualized, empirically supported therapy that is strongly focused on repairing adult attachment bonds. We sought to examine a neural index of social emotion regulation as a potential mediator of the effects of EFT. Specifically, we examined the effectiveness of EFT for modifying the social regulation of neural threat responding using an fMRI-based handholding procedure. Results suggest that EFT altered the brain's representation of threat cues in the presence of a romantic partner. EFT-related changes during stranger handholding were also observed, but stranger effects were dependent upon self-reported relationship quality. EFT also appeared to increase threat-related brain activity in regions associated with self-regulation during the no-handholding condition. These findings provide a critical window into the regulatory mechanisms of close relationships in general and EFT in particular.

The social regulation of threat-related attentional disengagement in highly anxious individuals.

Social support may normalize stress reactivity among highly anxious individuals, yet little research has examined anxious reactions in social contexts. We examined the role of both state and trait anxiety in the link between social support and the neural response to threat. We employed an fMRI paradigm in which participants faced the threat of electric shock under three conditions: alone, holding a stranger's hand, and holding a friend's hand. We found significant interactions between trait anxiety and threat condition in regions including the hypothalamus, putamen, precentral gyrus, and precuneus. Analyses revealed that highly trait anxious individuals were less active in each of these brain regions while alone in the scanner-a pattern that suggests the attentional disengagement associated with the perception of high intensity threats. These findings support past research suggesting that individuals high in anxiety tend to have elevated neural responses to mild or moderate threats but paradoxically lower responses to high intensity threats, suggesting a curvilinear relationship between anxiety and threat responding. We hypothesized that for highly anxious individuals, shock cues would be perceived as highly threatening while alone in the scanner, possibly due to attentional disengagement, but this perception would be mitigated if they were holding someone's hand. The disengagement seen in highly anxious people under conditions of high perceived threat may thus be alleviated by social proximity. These results suggest a role for social support in regulating emotional responses in anxious individuals, which may aid in treatment outcomes.

Childhood maternal support and social capital moderate the regulatory impact of social relationships in adulthood.

For this functional magnetic resonance imaging (fMRI) study, we assessed the impact of early social experiences on the social regulation of neural threat responding in a sample of 22 individuals that have been followed for over a decade. At 13 years old, a multidimensional measure of neighborhood quality was derived from parental reports. Three measures of neighborhood quality were used to estimate social capital-the level of trust, reciprocity, cooperation, and shared resources within a community. At 16 years old, an observational measure of maternal emotional support behavior was derived from a mother/child social interaction task. At 24 years old, participants were asked to visit our neuroimaging facility with an opposite-sex platonic friend. During their MRI visit, participants were subjected to the threat of electric shock while holding their friend's hand, the hand of an anonymous opposite-sex experimenter, or no hand at all. Higher adolescent maternal support corresponded with less threat-related activation during friend handholding, but not during the stranger or alone conditions, in the bilateral orbitofrontal cortex, inferior frontal gyrus and left insula. Higher neighborhood social capital corresponded with less threat-related activation during friend hand-holding in the superior frontal gyrus, supplementary motor cortex, insula, putamen and thalamus; but low childhood capital corresponded with less threat-related activation during stranger handholding in the same regions. Exploratory analyses suggest that this latter result is due to the increased threat responsiveness during stranger handholding among low social capital individuals, even during safety cues. Overall, early maternal support behavior and high neighborhood quality may potentiate soothing by relational partners, and low neighborhood quality may decrease the overall regulatory impact of access to social resources in adulthood.

Implicit conditioning of faces via the social regulation of emotion: ERP evidence of early attentional biases for security conditioned faces.

Not much is known about the neural and psychological processes that promote the initial conditions necessary for positive social bonding. This study explores one method of conditioned bonding utilizing dynamics related to the social regulation of emotion and attachment theory. This form of conditioning involves repeated presentations of negative stimuli followed by images of warm, smiling faces. L. Beckes, J. Simpson, and A. Erickson (2010) found that this conditioning procedure results in positive associations with the faces measured via a lexical decision task, suggesting they are perceived as comforting. This study found that the P1 ERP was similarly modified by this conditioning procedure and the P1 amplitude predicted lexical decision times to insecure words primed by the faces. The findings have implications for understanding how the brain detects supportive people, the flexibility and modifiability of early ERP components, and social bonding more broadly.

A semi-parametric model of the hemodynamic response for multi-subject fMRI data.

A semi-parametric model for estimating hemodynamic response function (HRF) from multi-subject fMRI data is introduced within the context of the General Linear Model. The new model assumes that the HRFs for a fixed brain voxel under a given stimulus share the same unknown functional form across subjects, but differ in height, time to peak, and width. A nonparametric spline-smoothing method is developed to evaluate this common functional form, based on which subject-specific characteristics of the HRFs can be estimated. This semi-parametric model explicitly characterizes the common properties shared across subjects and is flexible in describing various brain hemodynamic activities across different regions and stimuli. In addition, the temporal differentiability of the employed spline basis enables an easy-to-compute way of evaluating latency and width differences in hemodynamic activity. The proposed method is applied to data collected as part of an ongoing study of socially mediated emotion regulation. Comparison with several existing methods is conducted through simulations and real data analysis.

Familiarity promotes the blurring of self and other in the neural representation of threat.

Neurobiological investigations of empathy often support an embodied simulation account. Using functional magnetic resonance imaging (fMRI), we monitored statistical associations between brain activations indicating self-focused threat to those indicating threats to a familiar friend or an unfamiliar stranger. Results in regions such as the anterior insula, putamen and supramarginal gyrus indicate that self-focused threat activations are robustly correlated with friend-focused threat activations but not stranger-focused threat activations. These results suggest that one of the defining features of human social bonding may be increasing levels of overlap between neural representations of self and other. This article presents a novel and important methodological approach to fMRI empathy studies, which informs how differences in brain activation can be detected in such studies and how covariate approaches can provide novel and important information regarding the brain and empathy.

Nonparametric inference of the hemodynamic response using multi-subject fMRI data.

Estimation and inferences for the hemodynamic response functions (HRF) using multi-subject fMRI data are considered. Within the context of the General Linear Model, two new nonparametric estimators for the HRF are proposed. The first is a kernel-smoothed estimator, which is used to construct hypothesis tests on the entire HRF curve, in contrast to only summaries of the curve as in most existing tests. To cope with the inherent large data variance, we introduce a second approach which imposes Tikhonov regularization on the kernel-smoothed estimator. An additional bias-correction step, which uses multi-subject averaged information, is introduced to further improve efficiency and reduce the bias in estimation for individual HRFs. By utilizing the common properties of brain activity shared across subjects, this is the main improvement over the standard methods where each subject's data is usually analyzed independently. A fast algorithm is also developed to select the optimal regularization and smoothing parameters. The proposed methods are compared with several existing regularization methods through simulations. The methods are illustrated by an application to the fMRI data collected under a psychology design employing the Monetary Incentive Delay (MID) task.

Of snakes and succor: learning secure attachment associations with novel faces via negative stimulus pairings.

Integrating ideas from Mikulincer and Shaver's (2003) process model of attachment and Nelson and Panksepp's (1998) neurobiological theory of an integrated social emotion system, we predicted novel attachment-related learning effects. In two experiments, we tested for a unique form of conditioning based on the social regulation of emotion. Consistent with this theoretical integration, the results indicated that people develop more positive and less negative associations with faces of people who display genuine smiles if those faces have been implicitly paired with a distressing stimulus (e.g., a striking snake). These findings could have broad implications and should be of interest to researchers who study attachment, social and affective neuroscience, emotion, learning and memory, attitudes, and interpersonal relationships.