Towards the Epigenetics of Human Attachment

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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“.

HPA

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.

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

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

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Shyness and Humor Processing in Children

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.

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

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.

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Attachment Style and Brain Activity in Adolescents

This blog post first appeared on www.huffingtonpost.com on July 31, 2014.

 

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Adolescence is a critical time period during human social-emotional development. It is generally associated with changes in teenagers’ brain structure and function, as well as behavior. There is, however, also a major environmental change occurring during adolescence that is less frequently mentioned in this context, namely the separation of adolescents from their family. During teenage years, time spent with family members drops while time spent with people outside the family context (e.g., peers, work colleagues, romantic partners, etc.) increases. This social-adaptation process requires adolescents not only to integrate new and diverse experiences in relation to the world and themselves but to resolve many disagreements and interpersonal conflicts. In a nutshell, one of the central developmental tasks teenagers are confronted with is the establishment of an accurate understanding of their changing social environment.

Being a social neuroscientist particularly interested in human attachment behavior and attachment style, one of my research goals is to better understand the neural underpinnings of the above-described social-adaptation process in adolescents from an attachment-theory perspective. In other words, I am asking the question of whether a teenager’s attachment orientation (or attachment style) — which is established early in life through interactions between children and their primary caregiver(s) — could potentially explain individual differences in how adolescents’ brains process social-emotional information. Despite the fact that we already know quite a bit about the neural signature of attachment insecurity in adults, it still remains largely unknown what a neural signature of attachment insecurity may look like in teenagers. Together with a group of researchers from the University of Geneva — including David Sander, Brittany Anderson, Deborah Badoud, Stephan Eliez and Martin Debbane — we therefore measured social-emotional brain activity in 33 healthy adolescents ages 12 to 19 by means of functional magnetic resonance imaging (fMRI) and also obtained measures of their attachment style. The corresponding paper has just been published and is freely available here.

FIGURE_1The adolescents’ task in the fMRI scanner consisted of rapidly detecting on which side of a white line there were more dots (see figure, part a). More important, however, was the feedback adolescents obtained after each trial (see figure, part b). The latter feedback was composed of a word (either “won” in case of a correct answer, or “lost” in case of an incorrect answer) and an emotional facial expression (either smiling or angry). While two feedback combinations were congruent (smiling face and word “won,” angry face and word “lost”), two feedback combinations were incongruent (smiling face and word “lost,” angry face and word “won”). This setup allowed us to investigate adolescents’ brain responses while they were integrating objective performance feedback (personal success vs. failure) with the social evaluation of their performance (emotional faces representing social support vs. disapproval). We refer to this integration as social-feedback processing.

Our main findings indicate that attachment insecurities in adolescents may be associated with individual differences in brain activation during social-feedback processing. Furthermore, such individual differences appear to be distinct as a function of avoidant vs. anxious attachment orientations. We found that attachment avoidance was linked to increased brain activity during congruent social feedback processing. In other words, avoidantly attached adolescents appeared to preferentially process social feedback confirming their objective task performance. Conversely, we found that attachment anxiety was associated with increased brain activity during incongruent social-feedback processing. The higher adolescents scored on attachment anxiety, the more they seemed to focus on social feedback that did not match their objective task performance.

During adolescence, adaptively responding to one’s (changing) social context appears to involve a certain sensitivity and openness to socially conflicting information. Our new fMRI data suggests that, on a neural level, teenagers with an insecure attachment style may process social conflict differently from their securely attached peers. In the case of attachment avoidance, our data indicate that social conflict may be given less attention (i.e., social conflict is avoided). In turn, in the case of attachment anxiety, social conflict may be given too much attention (i.e., social conflict is overrepresented). Both of these social-conflict processing strategies have the potential to interfere with successful interpersonal-conflict resolution and social learning.

High levels of perceived social conflict are consistently associated with children, adolescents, and young adults manifesting psychological distress and maladjustment. We therefore believe that confirming and extending our findings is of high potential (clinical) relevance. Future investigations should also address the question of how such altered social-emotional brain-activation patterns as a function of attachment insecurity in adolescents are related to the neural signature of attachment insecurity emerging in adults. Combining such knowledge will hopefully support the development of new (early) detection and intervention strategies in the context of attachment insecurity.

 
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The Neural Signature of Attachment Insecurity

This blog post first appeared on www.huffingtonpost.com on October 16, 2013.

 

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In one of my previous blog posts on human social brain evolution, I already briefly mentioned the concept of attachment and attachment style. Here, I would like to elaborate on these considerations by describing in more detail what we have learned about the neural mechanisms underlying attachment behaviors in humans, and how such information could help us maintain better relationships with others.

In the late 1960s and early 1970s, Mary Ainsworth and John Bowlby first described a developmental psychological framework related to social interactions that has since become known as attachment theory. It states that, in order to survive, infants form a strong bond to their primary caregiver(s); they become attached. As infants grow older, this attachment evolves from a primarily biologically driven “survival instinct” into a sophisticated “cognitive-emotional social relationship processor.” A person’s mode of attachment, also called attachment style, determines what he/she will expect from social interactions, and how she/he will use cognitive and emotional resources for self-regulation during times of social emotional stress.

Central to the understanding of the concept of attachment is the assumption that all infants will become attached, but that such attachment can be either secure (i.e., “good”) or insecure (i.e., “bad”). It all depends on how the primary caregiver(s) respond to the infant’s attempts to establish a close social connection. Ideally, the caregiver(s) are available, responsive and caring in times of need. Infants consequently learn to trust in others and their own social emotional abilities; they can establish a secure attachment style. Unfortunately, such scenario does not always happen, allowing for the formation of an insecure attachment style in infants. If the primary caregiver(s) react in an unpredictable or inconsistent manner to the infant’s social approach signals, an anxious attachment style is bound to emerge. The latter is characterized by a constant fear of abandonment and need for reconfirmation due to a very low self-esteem. In turn, if the primary caregiver(s) is/are unavailable or unresponsive in times of need, infants will develop an avoidant attachment style. They learn to expect social rejection and fail to associate social interactions with positive experiences. Interacting with others may even be seen as futile or dangerous. Consequences are social-emotional closure and the denial for the need of social relationships. Some more information can also be found in blogs by Lisa Firestone (for example here).

Although the foundations of a person’s (secure versus insecure) attachment style are laid early in life, this process can have a strong influence on social emotional abilities and well-being throughout the lifespan, and even affect future generations. This comes from the fact that an individual’s attachment style is thought to remain rather stable from childhood to adolescence and adulthood, and may be transmitted from one generation to the next. Given that at least one third of people are believed to have an insecure attachment style and attachment insecurity is a known risk factor for the emergence of psychopathology (e.g., social anxiety disorder, or borderline personality disorder), attachment insecurity has a high potential for causing considerable problems in society.

In order to develop new detection, prevention and intervention strategies for social emotional difficulties associated with attachment insecurity, researchers have recently begun to investigate the neural basis of attachment style in humans. The main goal of such approach is to find neural markers of attachment insecurity in the human brain, allowing for understanding what may cause people to react with avoidance or anxiety to social emotional signals. Because it is easiest to establish such brain-behavior associations in adults, initial research has focused on adult populations.

Let’s first consider attachment anxiety. Converging evidence from adults suggest that this insecure attachment style is characterized by hyper-sensitivity to social emotional information in general, particularly so if negative. Anxiously attached individuals show high activity in brain areas that normally process social rejection and conflict, as well as maintain high arousal and negative emotionality. It looks as if anxiously attached people’s brains are constantly in a high alert state, monitoring the environment for potential signs of social emotional threats. Even if there are none.

Attachment avoidance, in turn, seems to considerably lower the brain’s responsiveness to social emotional information, especially so if positive. Avoidantly attached individuals show low activity in brain areas that usually process reward and prosocial motivation. This even appears to hold true for mothers seeing pictures of their own smiling infants, normally representing very potent inducers of reward-related social brain activity. It appears as if avoidantly attached individuals do not feel good when interacting with others. Even if these interactions are mutual.

Although admittedly reductionist (see here for more details), the above simplified description of the neural basis of attachment anxiety and avoidance nicely illustrates the strong influence the environment within which a person grows up in can have on social emotional brain responses during adulthood. These findings in humans furthermore nicely accord with data from animal studies (see here and here), the latter suggesting that such environmental effects can even override potential genetic predispositions for attachment insecurity.

The practical implications of the above-mentioned brain activations associated with attachment anxiety and avoidance are manifold. Firstly, we should be strongly aware of the fact that our behavior towards infants (as well as children and adolescents) can crucially influence their social emotional brain development, shaping how they themselves will behave during adulthood. Key elements of such awareness should be the maintenance of a stable, predictable and responsive environment within which children grow up in. Second, and associated with the first point, we should be more aware of our own attachment style to better understand our own reactions in the course of social interactions. This can help us to proactively change our social emotional behavior, or at least disengage from interactions early enough to prevent damage. And third, knowing more about the brain basis of attachment anxiety and avoidance, we can start developing new prevention and intervention strategies specifically targeting affected social emotional reward and threat behaviors and underlying brain circuits.

Ongoing research on the neural basis of attachment insecurity in adolescents and children will hopefully soon add more information, allowing for an early detection and prevention of, and/or intervention in the case of social emotional problems associated with attachment insecurity. The sooner we can act, the better.

 
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Tickling the Child Brain

This blog post first appeared on www.huffingtonpost.com on October 2, 2013.

 

laughing child

 

Not too long ago, there was a vivid debate on the evolutionary origins and function of humor in humans (HuffPost TEDWeekends; see herehere and here). I do agree that these are important questions to ask. I do also agree that, in order to answer these questions, we need more direct evidence on how humor is processed by the human brain. Luckily, thanks to modern neuroscience methods like functional resonance imaging (fMRI), we can nowadays look into the human brain right at the moment when it is exposed to something (deemed) funny. And that’s exactly what we did in a study yielding two recently published papers (paper 1 and 2): we tickled the child brain!

The experimental setup we used was simple. Our participants, who were 6 to 13 years old children, watched different kinds of short movies while their brains were scanned with fMRI. Movie clips were funny, positive (enjoyable to watch but nonfunny) or neutral, and funny movies contained scenes typically shown in the TV show America’s Funniest Home Videos. Our humor condition thus contained what Peter McGraw and Joel Warner would probably call “benign violations“: unsettling and/or threatening, but still acceptable and safe scenes.

The results of our manipulation revealed that the child brain processes humor very similarly to the adult brain, and thus mainly in two separate (but interconnected) networks. One set of areas is most likely involved in detecting and resolving the “benign violations”, or in our words “incongruity” that arises during humor processing. Such incongruity detection and resolution then likely entails a sense of amusement or mirth, reflected in increased activation of another set of brain structures associated with reward. This activation pattern reflects the latest “neural circuit model of (verbal) humor processing“ proposed by Chen and colleagues, which builds on Wyer and Collins’ original “comprehension and elaboration theory of humor“.

Besides confirming and further extending our knowledge of the neural substrates of humor processing in humans, our two child studies also tested for the influence of four additional variables. These were sex, intelligence, age, and temperament/personality.

The first two of these four variables, sex and intelligence, are particularly relevant from an evolutionary point of view, because one humor theory suggests that humor in humans might have evolved to serve as a tool for mate choice. More extensively explained in another blog, this theory proposes that women may use humor as a tool to evaluate men’s intelligence, resiliency, and/or social skills. Combined with previously acquired data from our laboratory in adults, our first paper in children may provide support for this mate choice theory. We found significantly stronger activity to humor in incongruity detection and resolution as well as reward areas in girls as compared to boys. These results imply that the female brain may be better prepared to perceive humor. One possible underlying mechanism for such humor predisposition in girls and women could be a weaker reward expectation, the latter appearing to be stronger in boys and men.

Although interesting, such sex-differences in humor processing related with the evolutionary aspect of mate choice do not provide any clues on a possible association with intelligence. That is why, in our second paper, we looked at neural response to humor as a function of IQ. Our findings again seem to support the mate choice theory, because we observed higher brain activity in both above-described networks with increasing IQ scores (across both sexes). It therefore appears that a higher IQ may not only facilitate incongruity detection and resolution, but also enhance the experience of amusement following it. As preliminary as our findings regarding intelligence are, they offer a good starting point for future scientific ventures, and represent a first putative link between humor theories and neural mechanisms associated with humor processing.

Apart from such evolutionary considerations related to sex and IQ, we also probed for the effects of age and temperament on humor processing in the second paper. Our results revealed that humor appears to undergo developmental changes, and that its neural signature is subject to individual differences in personality. It therefore seems that, although our brains may be to some degree predisposed to process humor, such humor processing can vary. For example, combined with previous data from children, we found that increasing age was associated with less reward-related, but more incongruity detection and resolution related brain activity. It could therefore be that older children process “benign violations” in a more elaborate way, less dependent on the fundamental safety and play nature of humor. Such findings corroborate a suggested differentiation between more basic, so-called “protohumor”, and more complex “formal humor”, the latter depending more strongly on theory of mind and language skills.

Finally, in our second paper, we observed that humor is susceptible to differences in personality. Of particular interest was the finding of weaker brain activity to humor in both incongruity processing and reward-related areas in shy children. Shy children are generally described as taking a long time to warm up to strangers, having difficulties with making friends, and not being very sociable. Such a personality trait may therefore hinder children to learn understanding and experiencing humor through social interactions. Consequently, shy children may have difficulties in detecting and resolving “benign violations”, because they do not have enough opportunities to learn what a “benign violation” actually is. In addition, shy children may experience social interactions as uncomfortable or “unsafe”, which could prevent shy children from interpreting them as “benign” from the start. These mechanisms might partially explain the increased risk for fearfulness and anxiety disorders, as well as proneness to peer rejection and victimization of shy children.

Overall, our findings on the neural basis of humor processing (in children) may provide some preliminary clues informing theories regarding humor evolution and function in humans. More fMRI and related neuroimaging research is, however, needed to reproduce and elaborate such considerations. This process may not only keep advancing humor theories, but could also be of clinical relevance for conditions involving social disturbances.

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