Bio-Behavioral Synchrony during Parent-Child Interaction and its potential Link to Attachment

Posted on January 18, 2019 by

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Social neuroscience, devoted to studying how biological systems implement social processes and behavior, has revealed crucial insights into the inherently social nature of humans. Most of the so far available findings, however, are derived from investigations examining biological processes and brain activation patterns in participants who were presented with social stimuli while being alone. Because “social cognition is fundamentally different when we are in interaction with others rather than merely observing them” (Schilbach, 2013), there currently is a strong motivation to implement truly interactive “second-person” social neuroscience paradigms to overcome this  limitation. 

One promising way to observe two individuals directly interacting with each other using state-of-the-art social neuroscience techniques is to apply functional near-infrared spectroscopy (fNIRS). fNIRS measures blood-oxygen-level dependent (BOLD) signal change as an indirect correlate of brain activity with the help of infrared light absorption. Although fNIRS can only reach the cortical surface, it offers many advantages over other neuroimaging techniques. Among others, it is minimally invasive, relatively motion insensitive, has a reasonably good spatial and temporal resolution, and allows for much more ecologically valid experimental setups. Furthermore, besides measuring change in brain activity in each participant separately, fNIRS hyperscanning – combined with behavioral ratings of videos recorded during interaction – allows to derive measures of bio-behavioral synchrony. In other words, fNIRS can be used to determine whether brain activity during social interaction shows a similar pattern in the same brain area(s) in both participants at the same time, and whether such increase in inter-brain coherence is associated with behavioral attunement and/or better behavioral task performance. 

But why are inter-brain coherence and bio-behavioral synchrony during social interaction of interest? The general idea is that for successful social interaction, the oscillatory processes in the interacting individuals’ brains have to become synchronized to each other so that information of any sort can flow between them – “analogous to a wireless communication system in which two brains are coupled via the transmission of a physical signal (light, sound, pressure or chemical compound) through the shared physical environment” (Hasson et al., 2012). Within this context, interpersonal synchrony is not only considered important at the neural (i.e. inter-brain coherence), but also at the behavioral (e.g. eye gaze, touch), physiological (e.g. heart rate), and endocrine (e.g. cortisol or oxytocin secretion) levels (Feldman, 2017). And this is where attachment comes into play. Social synchrony is learned within the parent-infant bond, which means that attachment contexts provide the arena for the experience and encoding of synchrony early in life. Furthermore, it is thought that social synchrony experienced during early sensitive periods provides the foundation for the expression of synchrony in later attachment bonds throughout the life span (Kinreich et al., 2017). For the emergence of attachment, however, it appears that not only social synchrony is of great importance. What also seems to be crucial are experiences of asynchrony as deviations from allostasis (and a subsequent return to synchrony and thus allostasis) – e.g. when a child becomes upset and the parent tries to calm her/him down. These sequences of synchrony, asynchrony, and re-synchrony provide ideal opportunities for the child to learn about the social environment, allowing him/her to start building predictions about the own capacity to elicit care and the responsiveness of others to help co-regulating emotions when needed (Atzil et al., 2018).

We are currently running a series of investigations along the above lines, during which we assess bio-behavioral synchrony in parent-child dyads (using fNIRS and behavioral rating of interaction videos) involving both mothers and fathers together with their children (CARE Studies). The results from an earlier study conducted at Stanford University in 28 mother-child pairs (child age 8-12 years) have just been accepted for publication (see here and publications page).

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Figure 1: Synchrony findings (adapted from Miller, Vrticka et al., 2019)

In this study, we show that inter-brain coherence in mother-child pairs generally increases across a set of four right prefrontal and one right lateral temporal cortical brain area(s) during a collaborative versus an independent visual reaction time task (see Figure 1, panels A and B) – particularly so in the dorsolateral and frontopolar prefrontal cortex (see Figure 1, panels A and C). Moreover, we report an overall sex-difference in this pattern, because differential inter-brain coherence was only present in mother-son but not mother-daughter dyads (see Figure 1, panel D). Our study is among very few to date reporting inter-brain coherence during mother-child interaction, and the first to show sex-differences in these patterns. Due to the preliminary nature of our findings, however, it is difficult to provide a concluding interpretation, particularly regarding the observed sex-differences. Although sex-differences in inter-brain coherence during cooperation have been found before in adult-adult dyads (Baker et al., 2016; Cheng et al., 2015), the so far available results do not converge yet and may reflect different underlying neural processes as compared to in parent-child dyads. More research is needed to replicate and further extend the parent-child data, for example by also including father-child interactions.

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Figure 2: Synchrony x Attachment findings (adapted & extended from Miller, Vrticka et al., 2019)

What we also tried for the first time in the above study is to associate bio-behavioral synchrony, and particularly inter-brain coherence during mother-child interaction, with a measure of parent-child attachment. To do so, we obtained child attachment towards the mother using a validated child version of the Experiences in Close Relationships self-report questionnaire in its revised version (ECR-R; ECR-RC). Associations between inter-brain coherence and child attachment towards the mother in this study, however, remain inconclusive. Although there was weaker inter-brain coherence increase during collaboration (versus the independent condition) in dyads within which children reported having a more avoidant attachment style towards their mothers in one area of the right frontopolar prefrontal cortex (p= .038; see Figure 2, panels A-C), this association did not survive correction for multiple comparisons and seemed to also partially depend on mother age and/or child gender. More research is therefore clearly needed to further extend our knowledge on inter-brain coherence and its association with attachment in the mother- and also father-child interaction. 

We are aiming at clarifying several of the above-mentioned  issues by performing fNIRS hyperscanning in larger samples of both mother-child and father-child pairs (child age 5 years, both girls and boys), and by obtaining attachment using several different procedures in both parents and children within our CARE studies. We hope that data from these additional studies will provide more information about the biological and brain basis of social interaction in general, and parent-child interaction in particular, and its potential links to parent-child relationship quality & attachment.

Original article:
Miller, J. G.*, Vrtička, P.*, Cui, X., Shrestha, S., Hosseini, S. M. H., Baker, J. M., Reiss, A. L. (2019; available online 27 December 2018). Inter-Brain Synchrony in Mother-Child Dyads During Cooperation: An fNIRS Study. Neuropsychologia, 124, pp. 117–124. (*= these authors share first authorship). [link]

 

Posted in Attachment, Brain Imaging, Neuroscience, Parent-Child Interaction, Psychology | Leave a comment

21st Century Attachment Theory and Research: Embracing a Social Neuroscience Approach

Posted on December 11, 2018 by

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On November 29th 2018, Ross Thompson and Heidi Keller were invited to the 2. Wilhelm Wundt Dialog on the topic of “Attachment Theory: Past, Present and Future” at the University of Leipzig. First as speakers and then as discussants, they deliberated about the current state of the field and how it has evolved since its inception in the 1950s. Furthermore, Thompson and Keller reflected on some of the remaining questions and unresolved issues of attachment theory and research, and how the latter could be addressed in the years and decades to come.

The Dialog inspired me to think more about possible future avenues of 21st century attachment theory and research. In this blog post, I would like to suggest that at least some of the remaining questions and unresolved issues could be addressed by embracing a social neuroscience approach – and by fruitfully combining it with already well established methods from the field in multi-method projects. But before elaborating on my suggestion, let us first have a look at some of the remaining questions and unresolved issues of attachment theory and research that were raised during the Dialog.

Remaining questions and unresolved issues

Who qualifies as an attachment figure – conceptual models of attachment. Original attachment theory postulated a strong attachment hierarchy, or even monotropy,  in conceptual attachment organization. In the monotropy model, the primary attachment figure (generally the mother) is thought to have an exclusive impact on children’s personality development despite the presence of other attachment figures. Similarly, the hierarchy model still attributes the best predictive value regarding child development to the primary attachment figure (again usually the mother), but acknowledges that relationships with subsidiary attachment figures (like the father) may also contribute, although to a lesser extent. These two initial models have recently been challenged, because the family structure has considerably changed since the 1950s. For example, fathers are nowadays regarded as important attachment figures, and their contribution to child development is increasingly recognized. This development is reflected in the emergence of (at least) two alternative models of conceptual attachment organization. In the independence model, all attachment relationships are assumed equally important for children’s development, but predicted to each contributing in distinct developmental domains. In turn, the integration model suggests that the quality of all attachment relationships taken together as a whole is what optimally predicts children’s developmental outcomes. It is, however, still debated which of the more recent models may more adequately depict conceptual attachment organization, and recent empirical evidence still appears to partially support the hierarchy model as a valid alternative. 

How is attachment transmitted from one generation to the next – sensitivity hypothesis. Attachment theory is built upon the assumption that once a certain attachment orientation has been established during early life, this attachment orientation remains relatively stable during childhood, adolescence, and adulthood, and is then transmitted from one generation to the next. As the principle moderating variable of this intergenerational attachment transmission, attachment theory emphasizes parental, and particularly maternal sensitivity. Thus, attachment theory predicts that the strength of the association between the mother’s attachment security (measured by the adult attachment interview) and the child’s attachment security (measured by the strange situation procedure) will be principally mediated by maternal sensitivity. Many studies provide evidence for a role of maternal sensitivity in intergenerational attachment transmission, evidence that is further backed up by several meta-analyses. The persisting problem, however, is that the amount of variance in intergenerational attachment transmission explained by maternal sensitivity alone is relatively modest. It is therefore likely that other variables moderate intergenerational attachment transmission, or the process by which maternal attachment security affects developing security of attachment in the child, and these variables have still to be determined with more confidence. This persistent problem is therefore also referred to as the transmission gap. 

Secure attachment is good and insecure attachment is bad – competence hypothesis. Attachment theory also postulates that a secure attachment is prerequisite for healthy social and emotional development, or in other words, necessary to become a competent child, adolescent, and adult. Within this context, competence is equated to good emotion regulation abilities and healthy social functioning. In his original writings, John Bowlby quite strongly implies such competence development in relation to his maternal deprivation hypothesis by saying that “broken attachment leads to delinquency and affectionless psychopathy”. Although it is nowadays still recognized that insecure attachment may represent a risk factor for the development of mental health issues – such as social anxiety or borderline personality disorder –, insecure attachment is not automatically equated with detrimental developmental outcomes anymore. In contrast, the nature versus nurture debate and its investigation using genetic and particularly epigenetic methods has contributed to the view that any attachment, be it secure or insecure, represents a meaningful and thus appropriate adaptation to one’s immediate environment. For example, if a child grows up in a family setting where attachment figures are unavailable and unresponsive in times of need, the emergence of an avoidant attachment orientation in the child represents an adequate developmental adjustment. Furthermore, social defense theory, a more recent derivative of attachment theory, suggests that inter-individual variation in attachment may even have benefits at the group level. The idea is that groups that are composed of people with different attachment orientations will be more effective when dealing with threats and dangers (early detection, rapid response, and effective cooperation) than less heterogeneous groups. Thus, rather than looking at attachment security versus insecurity and the potential implications of this dissociation for emotional and social competence with a black versus white approach, more differentiated consideration is necessary.

Is attachment universal – cross-cultural similarities versus differences. Attachment theory was developed in, and mainly tested on individuals from western, educated, industrialized, rich, and democratic societies – in short, WEIRD cultures. Nonetheless, it claims universality in the sense that attachment should work the same way all around the world. Consequently, measuring attachment anywhere by relying upon, for example, the strange situation procedure, should yield comparable results. Furthermore, if the results from one country do not correspond to “the norm” – usually being mean values of secure versus anxious versus avoidant attachment style distributions from the US and/or Europe and thus WEIRD cultures –, these results are regarded as a deviation. It has been known for quite a while that the core hypotheses of attachment theory, comprising the sensitivity and competence hypotheses mentioned above, are interpreted differently in different cultures, as, for example, very nicely illustrated by Rothbaum and colleagues by a direct comparison between the US versus Japan. There are many implications of cross-cultural differences in attachment on various levels, comprising moral judgments about good and bad parenting. Future attachment research therefore needs more cross-cultural studies and to evaluate cross-cultural differences within the cultural contexts they are observed. In the words of Heidi Keller, “diversity needs to be recognized as the human condition, and the recognition of diversity is an obligation for better science as well as for improving people’s lives”.

Embracing a Social Neuroscience Approach

How can one or more of the above remaining questions and unresolved issues of attachment theory and research be further elucidated during the 21st century? I would like to suggest that one way of doing so is by embracing a social neuroscience approach. I think that investigating the putative biological and neural substrates of inter-individual differences in attachment can be fruitfully combined with already well-established attachment measures in multi-method projects, and that the thereby obtained results  are likely to reveal new insights with the potential to inform attachment theory. So far, I have three different avenues in mind.

Understanding the neural substrates of attachment in humans on a single-person level. By relying upon social neuroscience methods such as electroencephalography (EEG), positron emission tomography (PET), and  (functional) magnetic resonance imaging ([f]MRI), human brain function can nowadays be investigated with great temporal and/or anatomical detail. In the context of attachment, it therefore is possible to, for example, study how mothers neurally react to images of their own versus unknown children, how adolescents represent positive and negative attributes of themselves versus their best friend, or how adults regulate emotions induced by viewing social versus nonsocial, positive versus negative images and by using either cognitive re-appraisal or expressive suppression. Furthermore, we can nowadays look at brain structure and connectivity either at rest or pre versus post a certain task. Most importantly, all of the above data can be combined with measures of attachment to look at the influence of inter-individual differences in attachment on brain function, anatomy, and connectivity. Derived from findings of my own research and integrating data from other laboratories across the globe, Patrik Vuilleumier and I have proposed a first functional neuro-anatomical model of human attachment in 2012, a model that I am constantly extending and refining. The model postulates that there is no unified brain system devoted to human attachment, but that attachment rather recruits a large network of brain areas also involved in other social and emotional functions. Nonetheless, we specify two core systems either processing information rapidly, in a bottom-up, and sometimes even unconscious manner – termed emotional processing system –, or in a slower, top-down, deliberate, and conscious manner – termed cognitive processing system. We furthermore suggest that the emotional processing system can be divided into a (social) approach versus aversion module, and the cognitive processing system into an emotion regulation versus a mental state representation module. Accumulating evidence suggests that inter-individual differences in attachment security versus insecurity (i.e. anxiety versus avoidance) can be reliably mapped onto brain activation and deactivation, as well as anatomical and connectivity patterns within the above four modules. Most of these data, however, stem from adults and to a lesser degree from adolescents, meaning that data from children is still crucially lacking. Nonetheless, I think that by better understanding how inter-individual differences in attachment affect brain activity, anatomy, and connectivity in single persons across the life span, attachment theory can be further specified. This pertains to all of the above remaining questions and unresolved issues, as such approach will provide fundamental insights into attachment processes on the biological/neural level across domains – for example, in mothers versus fathers, in children of securely versus insecurely attached parents, children from different socioeconomic contexts or with different histories of early life adversities, and individuals from different cultures.

Understanding the neural substrates of attachment in humans on an interpersonal level. Besides measuring brain activity in single participants, recent technological development now allows us to simultaneously measure brain activity in two (or more) individuals. In so doing, a new potential variable empirically describing relationship quality has emerged: brain-to-brain- or inter-brain-synchrony (IBS). According to theory, very close relationships (i.e. parent-child or romantic relationships) should be characterized by high(est) IBS, and IBS should successively decrease as the closeness of the interacting partners decreases (i.e. to friends and strangers). Because relationship quality from an attachment theory perspective not only depends on closeness per se (i.e. how close two individuals are to each other generally speaking), but primarily on how such closeness is individually perceived, we hypothesize that there should be ample variation in IBS even within the above four relationship categories. Furthermore, there should not only be variation as a function of inter-individual differences in attachment in IBS during tasks that necessitate social interaction (i.e. collaboration), but also in the temporal sequence of IBS versus inter-brain-asynchrony (IBA). Such pattern of IBS versus IBA appears particularly relevant for the emergence of attachment at the first place, because children are especially prone to learn about the functioning of their inner and outer environment during times of allostasis deviation through, for example, co-regulation processes with attachment figures. The measurement of IBS and IBA should thus be of ample importance for further elucidating the sensitivity hypothesis, but also clarifying conceptual attachment organization and the competence hypothesis, and revealing potential cross-cultural similarities versus differences on an interpersonal level.

Understanding intergenerational transmission. Attachment orientation emergence is nowadays being understood as a prototypical gene by environment interaction. It therefore appears logical to study this process by using a method that can disentangle the effects of nature versus nurture. A recently developed method offering such opportunity is the analysis of epigenetic DNA modification. As shown in a seminal study in rats that either displayed high versus low maternal behavior (i.e. licking and grooming) towards their pups, maternal behavior in these pups (once they became mothers themselves) could be associated with inter-individual differences in methylation of the glucocorticoid receptor gene (NR3C1) linked to HPA-axis functioning, stress, and anxiety (see also here). Corresponding data in humans has only recently started to emerge, particularly in the context of inter-individual differences in attachment (see also here). Directly testing epigenetic change patterns in children from birth using longitudinal study designs will help determining additional factors important for intergenerational attachment transmission apart from parental (maternal) sensitivity, and likely reveal variance regarding these factors themselves, both within and between cultures.

Conclusions

Attachment theory and research have steadily evolved over the course of the last seventy years. Nonetheless, several questions and issues remain unresolved. I am suggesting that during the 21st century, a combination of well-established attachment measures with new research protocols applying social neuroscience methods promises to yield results that will contribute to important advances of the field. Such approach will require more extensive collaborative efforts not only between different research domains, but also between research groups from different countries and cultural backgrounds. As a 21st century attachment researcher, I am very much looking forward to the next years and decades to come – there are exciting times ahead of us!

Posted in Attachment, Brain Imaging, Epigenetics, Neuroscience, Psychology | Leave a comment

How does the human brain process social (versus nonsocial) emotional information? New evidence from an electroencephalography (EEG) study.

Posted on August 23, 2018 by

The human species is inherently social. From the moment of birth and throughout the entire life span, we depend on social interaction, care, and protection. This notion is nicely reflected by attachment theory and its derivative social defense theory. Both theories emphasize the fundamental human need for social connection and effective cooperation to deal with threat by utilizing the strength of numbers. Such strong reliance on social resources for survival, in combination with a continuous increase in the complexity of our social environment, is even thought to have driven the evolution of our unusually large brains (for body size) – as described by another prominent theory, the social brain hypothesis.

Against the above background, it is likely that the degree of information’s social content may constitute a fundamental and distinct stimulus dimension, which means the human brain may be highly sensitive to the mere presence of social information. Neuroimaging studies using functional magnetic resonance imaging (fMRI) or electroencephalography (EEG), however, have so far only sparsely looked at the specificity of social versus non-social information processing. This particularly holds true for studies also comprising other stimulus dimensions that may be intrinsically salient, as for example negative and/or positive emotional valence as compared to neutral content.

On a more theoretical level, the above question can be situated within the realm of appraisal theories of emotion, and particularly the component process model of emotion. This model suggests that incoming information is only (neurally) processed if it is relevant to the organism at a specific moment in time. The model furthermore suggests that stimulus relevance can be determined in terms of (i) novelty (i.e. suddenness, familiarity, and/or predictability), (ii) intrinsic pleasantness (i.e. negative vs. positive [vs. neutral] valence), and (iii) goal / need relevance (i.e. whether the assessed information accords to or obstructs the current goals and needs of the organism). Despite the intrinsic relevance of social information for humans, the component process model of emotion does not comprise a relevance check in terms of social versus non-social content.

In this EEG study, we sought to clarify how the human brain processes social versus non-social content of incoming information if the latter also contains different intrinsic pleasantness, i.e. is of positive or negative valence or comprises emotionally neutral content. To this end, n= 24 young healthy females were shortly (150 ms) presented with complex visual scenes and their scrambled counterparts while making a scrambled versus intact decision by button press.

The most important finding of our study was that two very early components of visual processing around 80-120 ms and 200-320 ms after stimulus onset showed evidence for an interactive assessment of social content and emotional valence. On the one hand, the first component, also termed P1 – associated with attention allocation during sensory processing in the extrastriate visual cortex – showed augmented amplitudes selectively for social positive (versus non-social positive) content. On the other hand, the second component, also named early posterior negativity (EPN) – reflecting enhanced sensory encoding resulting from involuntary capture of attention – showed larger positivities for social (as compared to non-social) content, with an apparent boost of particularly positive and neutral social information (see Figure 1 below). 

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Figure 1: a Grand average event-related potentials (ERPs), contrasted for all six experimental conditions, synchronized to stimulus onsets, at the P1 (upper panel) and EPN / posterior ROI (lower panel). b ERP mean amplitudes (with SEMs) during the four time windows of interest; ROI= region of interest, pos= positive, neg= negative, neu= neutral. Figure taken from Schacht & Vrticka, 2018.

The above findings provide evidence for a very early neural dissociation of social versus non-social content and therefore an additional relevance check. Furthermore, our data suggest that such early social content relevance check is carried out by integrating it with intrinsic pleasantness information from the very beginning of visual processing. What is particularly interesting, is the fact that neural encoding of information that is of a social nature with a positive emotional valence (P1) and later on also neutral content (EPN) appears to be boosted. This boost counteracts a strong and prolonged negativity bias that is evident from about 200 ms and that persists until (at least) 620 ms after stimulus presentation.  

The interactive pattern of social content and emotional valence processing as detected using EEG described above is highly consistent with previous data we have obtained from a study using fMRI. Furthermore, the anatomical source localization of the P1 and EPN effects using EEG strongly overlap with brain activation observed in the fMRI data – particularly for the social > non-social contrast during the EPN (see Figure 2). Such replication of the fMRI effects by EEG therefore further bolsters the validity and generalization of our results.

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Figure 2: Juxtaposition of the fMRI  (Vrticka et al., 2013 – top) and EEG findings (Schacht & Vrticka, 2018 – bottom). Top (fMRI): A-C Illustration of brain areas that show a social content by emotional valence interaction with the corresponding activation pattern D-F; FG= fusiform gyrus, STG= superior temporal gyrus, mOFC= medial orbitofrontal cortex. Bottom (EEG): B Scalp distribution of ERP effects within the P1 (left) and EPN (right) time windows, and C respective source localizations of the social > nonsocial ERP differences within these intervals. D ERP mean amplitudes (with SEMs) for the social by emotional content interaction within the P1 (left panel) and the EPN (right panel) time windows. Please note that the color code for the activation pattern illustration is inverted for the two studies. Figures taken from Vrticka et al., 2013 (top) and Schacht & Vrticka, 2018 (bottom).

Taken together, our novel EEG results suggest that relevance detection may occur already as early as around 100 ms after stimulus onset and may combine relevance checks not only examining intrinsic pleasantness/emotional valence, but also social content as a unique and highly relevant stimulus dimension. 

We are currently running a follow-up combined fMRI & EEG study to replicate and further extend the observed early social content by emotional valence interaction effects (mapping of fMRI and EEG data within the same participants).

Both the fMRI and EEG papers described above are published open access and are freely available (distributed under the terms of the Creative Commons Attribution 4.0 International License [http://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made).

Posted in Brain Imaging, Neuroscience, Psychology, Relevance | Leave a comment

Towards the Epigenetics of Human Attachment

Posted on March 16, 2018 by

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Attachment theory postulates that the establishment of attachment bonds represents an innate, biologically programmed behavior. Its biological function is to enhance the chances of survival in times of danger and need. Accordingly, (almost) all children become attached to survive. However, beyond such basic biological function associated with survival, attachment theory emphasizes the existence of considerable inter-individual differences in attachment quality. These inter-individual differences in attachment quality are usually captured through secure versus insecure – anxious and avoidant – attachment orientations, and are used to predict universal strategies to either draw near, or away, from significant others during situations of personal distress. 

Since Bowlby’s pioneering writings on the theory of attachment, attachment researchers have been intrigued by the question how secure versus insecure attachment orientations emerge during human development. The most plausible explanation considers both genetic and social factors, in that, as Jay Belsky puts it nicely in one of his blog posts: “it appears that some children are simply born secure, whereas others are made secure or insecure by, as theory would have it, the quality of rearing they experience“.

The above view that secure versus insecure attachment orientations emerge during development depending on both genetic and social factors was elegantly demonstrated by the seminal work of Weaver and colleagues in rats (original publications: 1999 and 2004). A comprehensive  and interactive online summary is available from the University of Utah Genetic Science Learning Center via the website  “Lick Your Rats“.

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In Weaver and colleagues’ work, the researchers selected rat mothers by naturally occurring inter-individual differences in maternal behavior, quantified by low versus high licking and grooming (LG) and arched-back nursing (ABN). Within this context, a high LG-ABN rat mother would most closely resemble a sensitive / available human mother and thus a rearing environment favoring the emergence of a secure attachment orientation in the offspring. In turn, a low LG-ABN rat mother would most closely resemble an insensitive / unavailable human mother and thus a rearing environment favoring the emergence of an insecure attachment orientation in the offspring.

The researchers then examined adult pups of low and high LG-ABN rat mothers that were either brought up by their own / biological mother, or reared by a foster mother. In so doing, the researchers found that some pups were “born secure” (i.e. adult pups from a high LG-ABN mother reared by a low LG-ABN foster mother resembled adult pups born and reared by a high LG-ABN mother), whilst others “were made secure by the quality of rearing” (i.e. adult pups from a low LG-ABN mother reared by a high LG-ABN foster mother resembled adult pups born and reared by a high LG-ABN mother). 

In addition to showing the above patterns based on observing the adult rat pups’ behavior, Weaver and colleagues also provided an underlying biological mechanism reflecting a gene by environment interaction. They found that the influence of the environment on pup development was maintained by non-genomic transmission of individual differences in terms of epigenetic DNA modification. Specifically, they observed that expression of the glucocorticoid receptor as important part of the HPA axis regulating stress was altered in rat pups through DNA methylation, thereby determining how strongly the rat pups responded to stress during adulthood. 

Since Weaver and colleagues reported the above findings in rats, some evidence for the same mechanism involving epigenetic modification of the glucocorticoid receptor has been found in humans postmortem (associated with childhood abuse). It therefore appears that both genetic and social factors also play a role in human development. A nice overall summary mentioning the experiments in low versus high LG-ABN rats, and more generally discussing the associated nature versus nurture debate in relation to human development, can be found in this YouTube video (University of Oslo).

According to the above-described theoretical considerations and animal data, we set out to investigate whether we could find evidence for a gene by environment interaction in association with attachment in humans. To this end, we turned to attachment theory and its assumption that inter-individual differences in attachment orientations can be used to  predict universal strategies to either draw near, or away, from significant others during situations of personal distress.

To capture the propensity to approach (or avoid) others, we used a biological marker associated with the oxytocin system, namely the oxytocin receptor gene (OXTR). As for the study in rats, we then also assessed the glucocorticoid receptor gene (NR3C1) associated with the HPA stress axis, and particularly the negative feedback loop to end the stress response. In both cases we looked at the degree of gene promoter methylation as a function of attachment security versus insecurity (i.e. attachment avoidance and anxiety), the latter obtained through an attachment self-report questionnaire. To analyze OXTR and NR3C1 promoter methylation, our participants – 109 young healthy adults (56 female) – provided saliva samples. 

rahd_a_1446451_f0002_bWhat we observed was a specific effect for attachment avoidance: the higher our participants scored on attachment avoidance (i.e. high levels of attachment avoidance with concomitantly low levels of attachment anxiety), the more OXTR and NR3C1 promoter methylation was present. Furthermore, we did not find any differentiation between attachment security and anxiety – they both were linked to similar levels of OXTR and NR3C1 promoter methylation. The same was true for a combination of high attachment anxiety and avoidance (fearful-avoidant).

Although these findings are preliminary and need replication and further extension, they tentatively suggest that attachment in humans could also be related to epigenetic DNA modification, particularly in two systems associated with the social regulation of stress. What is interesting is that attachment avoidance appears to be most strongly linked to OXTR and NR3C1 promoter methylation, with attachment avoidance most consistently showing links to diminished social responding and support-seeking in humans.

Caution is advised, however, when interpreting our findings, because they emerged from a correlational study and only reflect epigenetic DNA modification at one time point. We can therefore not establish any causal relationship between OXTR and NR3C1 promoter methylation and attachment (avoidance) in humans as of yet. These and some additional limitations are explicitly mentioned in the corresponding publication (see below).

Despite the currently present limitations, we think that the assessment of gene (promoter) methylation offers a promising new avenue to study gene by environment interactions in the context of human attachment, and hope that this approach may inform future prevention and intervention strategies. 

The above data were published in the following paper: 

Tsachi Ein-Dor, Willem J. M. I. Verbeke, Michal Mokry & Pascal Vrtička (2018). Epigenetic modification of the oxytocin and glucocorticoid receptor genes is linked to attachment avoidance in young adults. Attachment & Human Development.
DOI:  10.1080/14616734.2018.1446451.

Our paper is published open access and therefore freely available.

Posted in Attachment, Epigenetics, Neuroscience, Psychology | 1 Comment

The insecurely attached brain: How early social interactions can shape adult brain function

Posted on March 15, 2018 by
This blog post first appeared on http://thepeoplesscience.org/ on October 29, 2016.

 

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In a first review paper within the field, Patrik Vuilleumier and I recently proposed a model describing how attachment insecurities influence social brain function in healthy adults. It has been known for more than four decades that early social interactions can crucially shape social behavior throughout the lifespan. Evidence regarding the underlying neural mechanisms, however, has only started to emerge during the last years. Because attachment insecurities have a high prevalence, can be transmitted across generations, and increase the risk for social emotional disturbances, we hope our model can help advancing new prevention and treatment approaches.

Humans are a highly social species. We enjoy the company of friends and like sharing our personal experiences with others. Mutual social interactions and self-disclosure usually entail increased activity in our brain’s reward circuit: the very same network that is activated by basic reinforcers such as food or sex. It simply feels good to be social. Conversely, when we are socially excluded, activity increases in areas of our brain that mediate physical pain responses. Social rejection really does hurt.

In some people, however, these intrinsic links between social versus antisocial behavior and brain activity appear to be malfunctioning. Furthermore, such malfunction seems to trace back to unfavorable social interactions in early life. The brains of avoidantly attached healthy adults have been found to insufficiently activate, but the brains of anxiously attached adults to excessively respond to social and antisocial cues. Yet, what does it mean to be avoidantly or anxiously attached?

Attachment theory proposes that every child is born with an innate attachment system. Its biological function is to enhance survival through proximity seeking in times of need. Although all children become attached, their attachment can be insecure. In the case of attachment avoidance, children experience repeated interactions with unresponsive attachment figures. They therefore learn to expect social rejection and fail to associate social behavior with positive feelings. In the case of attachment anxiety, children experience repeated interactions with inconsistent attachment figures. Sometimes they are comforted by others, sometimes rejected, and this in an unpredictable way. As a consequence, anxiously attached children become overly sensitive to cues of social approval and disapproval.

Attachment theory furthermore states that these negative early attachment patterns remain rather stable during the lifespan. An insecure attachment style can thus influence social behavior and associated brain function from childhood through adolescence and adulthood. In addition, evidence summarized in our review paper indicates that attachment insecurities not only affect directly attachment-related processes (e.g., parent-infant relationships), but (almost) all social interactions, even with strangers.

Roughly 40% of individuals are insecurely attached. In addition, the plot thickens that attachment insecurities can be transmitted across generations. Insecurely attached people also run a higher risk for developing psychological and psychiatric disorders. A better understanding of the neural basis of an insecure attachment style therefore is of high general interest. If we learn how to successfully prevent and treat attachment insecurities, we can proactively increase the wellbeing of future generations.

The above described review paper appeared in Frontiers of Human Neuroscience, and is freely available here:

http://www.frontiersin.org/Human_Neuroscience/10.3389/fnhum.2012.00212/full

Posted in Attachment, Brain Imaging, Neuroscience, Psychology | Leave a comment

Shyness and Humor Processing in Children

Posted on March 15, 2018 by
This blog post first appeared on http://thepeoplesscience.org/ on October 29, 2016.

 

shyness

 

Humor is a prototypical positive social human state. It acts as a social glue, facilitating the initiation and maintenance of social relationships. Humor could even serve as a tool for human mate selection, providing women with information about men’s mating quality beyond what meets the eye. I have already mentioned these characteristics of humor in humans in one of my previous posts, in which the main focus was on sex-differences.

In a subsequent publication, Jessica Black, Michelle Neely, Elizabeth Walter Shelly, Allan Reiss and I looked at additional factors besides sex that could influence humor processing. Again relying on functional magnetic resonance imaging (fMRI) data from 22 children ages 6-13, we examined how the children’s age, intelligence and temperament could possibly affect children’s ability to cognitively (“getting the joke”), and/or emotionally (“feeling amused by the joke”) process humor. In order to do so, children were shown a series of short movie clips taken from the TV show “America’s Funniest Home Videos” during fMRI scanning, and were psychologically assessed. For a comprehensive account of our findings, please check out another of my blogs available here.

In the present post, I would like to focus on one specific result of the second paper, namely the influence of temperament, and particularly shyness, on humor processing in children. Shy children are usually described as feeling uncomfortable when being in novel social surroundings. Such social discomfort may explain why shyness is characterized by decreased sociability, longer time needed to warming up to strangers, and having difficulties with making friends. Consequently, shy children may have fewer chances for acquiring social skills necessary for interacting with others in a positive way. This lack of social experience could eventually explain why shy children are more vulnerable to developing anxiety disorders, and are more likely to experience peer rejection and victimization.

In our study, we found that brain activity related to humor processing was weaker the higher children scored on shyness. Such negative relation between brain activity to humor and shyness was present in several different brain areas known to be involved in both cognitive (“getting the joke”) and emotional (“feeling amused by the joke”) humor processing. It therefore appears that shy children may have difficulties in understanding humor and consequently feel less positively stimulated by it.

The above-mentioned observation of difficulties during humor processing in shy children may be of potential clinical relevance.  There is growing evidence that mutual social interactions importantly involve positive emotions associated with reward-related experiences. It usually feels good to be with others, and this good feeling makes us to repeatedly search for social interactions. In some cases, however, this social reward mechanism appears disturbed, as for example in people having an avoidant attachment style (see my previous post for more information), or in shy children as described here. Knowing more about how the human brain processes positive social information, and under which circumstances such processing may be impaired, could provide important clues for the development of future prevention and intervention strategies in clinical settings.

Posted in Brain Imaging, Humor, Neuroscience, Psychology | Leave a comment

Sex-Differences in Humor Processing: Potential Implications for Human Mate Choice?

Posted on March 15, 2018 by
This blog post first appeared on http://thepeoplesscience.org/ on October 29, 2016.

 

humor

 

A good sense of humor is a highly valued human mate preference worldwide. If people are asked to rate the importance of various traits of a potential partner, humor is often found at, or near the top of their list. Humor sometimes ranks even higher than physical attractiveness. Combined with previous research in adults, new functional magnetic resonance imaging (fMRI) data from children published in a recent paper by Michelle Neely, Elizabeth Walter Shelly, Jessica Black, Allan Reiss and I, could provide some preliminary clues on how humor relates to human mate selection.

Humor is a prototypical positive social human state. It is thought to have evolved from a basic safety and play signal, and is associated with smiling and laughter, two powerful and contagious social gestures. Not surprisingly, humor is known to act as a social glue, facilitating the initiation and maintenance of social relationships. Humor has also been found to have positive effects on physical and psychological wellbeing, probably because it offers a way for dissolving pent up stress and regulating negative emotions. Furthermore, humor has been associated with creativity and intelligence. This comes from the fact that both humor production and evaluation require the ability to combine two or more otherwise incompatible or incongruent elements. A good sense of humor therefore does not just equate to “being funny”; it could also indicate good social skills, resilience, as well as creativity and intelligence.

According to sexual selection theory, mate selection in mammals – including humans – is characterized by males competing for females’ attention. Because females invest more time and energy in childbearing and parenting, they are more restricted than males in the number of offspring they can conceive. As a consequence, females are highly selective in their mate choice. And here is where humor may come into play. Humor could serve as a mate selection tool because it provides women with information about men’s mating quality beyond what meets the eye. In turn, it gives men the opportunity to display their social skills, resiliency, creativity and intelligence in an agreeable and entertaining way.

Finally, if humor is one tool for selecting a potential mate, women’s and men’s brains could have evolved differentially to make use of this mechanism. Specifically, women’s brains may have developed a predisposition for evaluating humor, while men’s brains may have developed a different predisposition for producing humor. Our fMRI data from adults and more recently young children (ages 6-13) provides first preliminary evidence for such different predispositions in humor as a function of sex. A potential underlying neural mechanism might be related to reward anticipation. It appears that girls and women are less in a reward anticipation mode, which could make their brains better suited for evaluating humor.

Although our findings on sex-differences during humor processing are promising, many open questions remain. For example, we still do not know whether such results hold true for different kinds of humor. It is also likely that there are differences in humor processing related to cultural learning, which calls for cross-cultural studies on humor processing. And we are still in the need of more direct evidence for associations between brain activity during humor processing and measures of creativity, intelligence, and resilience. Future research will hopefully soon provide additional information on these and other open questions.

Posted in Brain Imaging, Humor, Neuroscience, Psychology | Leave a comment