INSIGHTS INTO THE NEURAL AND AFFECTIVE SIGNATURES OF CONNECTEDNESS BETWEEN PARENTS AND ADOLESCENTS I SEE YOU Mirjam C.M. Wever
I SEE YOU Insights into the neural and affective signatures of connectedness between parents and adolescents Mirjam C.M. Wever
Cover design: Evelien Jagtman | www.evelienjagtman.nl Lay-out: Wendy Bour-van Telgen Printed by: Gildeprint, Enschede, the Netherlands | www.gildeprint.nl ISBN: 978-94-6419-995-6 All research described in this dissertation was supported by the Netherlands Organization for Scientific Research (NWO) through a personal VICI-grant awarded to prof. dr. Bernet M. Elzinga (grant number: 453-15-006). Copyright © 2023 Mirjam C.M. Wever All rights reserved. No parts of this dissertation may be reproduced, stored, or transmitted in any form or by any means without written permission of the author.
I SEE YOU Insights into the neural and affective signatures of connectedness between parents and adolescents Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Leiden, op gezag van rector magnificus prof.dr.ir. H. Bijl, volgens besluit van het college voor promoties te verdedigen op donderdag 11 januari 2024 klokke 16.15 uur door Mirjam Cecilia Maria Wever geboren te Oosterblokker in 1991
Promotor Prof.dr. B.M. Elzinga Co-promotores Dr. G.J. Will Dr. M.S. Tollenaar Promotiecommissie Prof.dr. M.E. Kret Prof.dr. C.M. Keysers Universiteit van Amsterdam Prof.dr. N.J.A. van der Wee Dr. P.A. Bos
Voor mijn ouders De kleine dingen die jullie deden hebben me groot gemaakt.
TABLE OF CONTENTS Chapter 1 General introduction 9 Chapter 2 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others 23 Chapter 3 Looking into troubled waters: Childhood emotional maltreatment modulates neural responses to prolonged gazing into one’s own, but not others’, eyes 55 Chapter 4 Neural and affective responses to prolonged eye contact with parents and unfamiliar others in depressed and non-depressed adolescents 85 Chapter 5 Neural signatures of parental empathic responses to imagined suffering of their adolescent child 117 Chapter 6 Eyes on you: Ensuring empathic accuracy or signaling empathy? 155 Chapter 7 Summary and general discussion 183 Chapter 8 Appendices Dutch summary | Nederlandse samenvatting 204 References 217 About the author | Curriculum Vitae 245 List of publications 246 Acknowledgements | Dankwoord 249
1 Chapter 1 General introduction “The interaction between a parent and child can be like a dance. There are routines, standards and missteps, there is give and take, there is unparalleled intimacy, there are often vast differences in skill level and motivation, there is learning. A parent must learn to be an adept partner, being sensitive to the needs of their offspring while ultimately guiding the quality and nature of care to ensure normal growth and development. This dance can be beautiful. It can be tender. It can be awkward. It can be difficult. And sometimes it just does not occur.” (Barrett & Fleming, 2011) Chapter 1 General introduction “The interaction between a parent and child can be like a dance. There are routines, standards and missteps, there is give and take, there is unparalleled intimacy, there are often vast differences in skill level and motivation, there is learning. A parent must learn to be an adept partner, being sensitive to the needs of their offspring while ultimately guiding the quality and nature of care to ensure normal growth and development. This dance can be beautiful. It can be tender. It can be awkward. It can be difficult. And sometimes it just does not occur.”
10 Chapter 1 Parental caregiving is one of the most fascinating and best-preserved behaviors throughout evolution of mammalian species, humans included. It facilitates parents to perceive and appropriately respond to physiological and emotional cues from their offspring, signaling hunger, pain, or distress, therewith serving as an innate parental protection system (De Waal, 2008). As previously phrased by Barrett and Fleming (2011), parental caregiving can be described as a beautiful dance between a parent and child during which a parent learns to be adaptive and sensitive to the needs of their offspring. Concurrently, parents need to guide the quality and nature of this care to ensure normal growth and development of their offspring. Although this can be a challenge throughout all stages of development, adolescence is thought to be a specifically challenging period for parent-child dyads. This is due to the tremendous social, emotional, behavioral, and environmental changes adolescents encounter, which demands a different parental skillset compared to childhood. Parents need to adapt to these changes and need to find a new balance between being sensitive and responsive to the changing needs and emotional states of their adolescent child, while also giving appropriate guidance, and support their child’s ability to make autonomous decisions (Kobak et al., 2017). When all goes well, this will lead to a strong socio-emotional connection between a parent and child and a securely attached relationship, which fosters healthy socio-emotional development in the transition from childhood to adulthood (George & Solomon, 1999). However, flourishing in this task turns out to be a bigger challenge for some parent-child dyads than for others and several inter-individual factors are thought to affect this parent-child dance, demanding for an adjustment of the “dance steps” or the “rhythm”. During adolescence, parent-child dyads find themselves in a complex emotional landscape and, although not in every family, increases in the frequency and intensity of conflicts are more likely in this period than in others (Arnett, 1999; de Gelder et al., 2011; Restifo & Bögels, 2009; Shanahan et al., 2007). A factor likely contributing to these changes in family dynamics is the enhanced sensitivity to social evaluation in adolescents (Somerville, 2013), which gives rise to higher levels of affect lability and irritability (Steinberg & Silk, 2002). In addition, adolescents become more autonomous in this period and the relationship with their parents starts to take on a new, more egalitarian, form (Crone & Dahl, 2012). Altogether, the parent-adolescent relationship is put under pressure during this developmental period and parents and adolescents need to find a new balance in connecting with each other on a social and emotional level. This is important as, despite adolescents starting to spend more time with peers, they still perceive their parents as their most important advisors. This is in line with the fact that parental support remains a strong predictor of adolescents’ wellbeing and mental health (Baumrind, 1991; Yap et al., 2014), showing the ongoing importance of a strong parent-child bond during adolescence. Feeling connected with others on a socio-emotional level can be defined as a deep bond that is formed between people, which made them feel loved, cared for, and valued by the other
1 11 General introduction (Eisenberger & Cole, 2012). Strong social connections with others are crucial for one’s mental and physical well-being, and are thought to be even more important for a strong parent-child bond (Ainsworth et al., 1978; Bowlby, 1969). As such, it is hardly surprising that negative social experiences (e.g., childhood emotional maltreatment) or circumstances that negatively affect (the perception of) these social connections (e.g., adolescent depression) may cause disturbances in the ability to interact with others, both within and outside the parent-child context. Extending our knowledge about neural and affective processes underlying this socio-emotional connection between parents and adolescents in well-functioning families may serve as a strong foundation for the understanding of difficulties and disturbances in this connectedness in dysfunctional family systems in which the parent-child bond may be at stake. Moreover, this will pave the way for the development of suitable interventions focusing on repairing this connection between parents and adolescents, which will potentially limit further harm due to family dysfunction. This thesis aimed to elucidate the neural and affective signatures of socio-emotional connectedness between parents and their adolescent child. This was operationalized by the assessment of two key processes in parent-child interactions: Eye contact and empathy. These two processes are highly important for the parent-child bond. Moreover, I further aimed to investigate two inter-individual characteristics that may explain differences in parents’ and adolescents’ ability to connect with each other on a socio-emotional level: A history of childhood emotional maltreatment in parents and adolescent depression. In order to do this, several behavioral and functional magnetic resonance imaging (fMRI) paradigms were used with a multimethod approach, including self-report measures of affective responses, functional neuroimaging assessed by blood-oxygen-level-dependent (BOLD-)activation in the brain, and gaze responses assessed with eye-tracking. This not only enabled us to examined how parents and adolescents feel, but also how they respond at the level of their gaze and brain when connecting with each other (see Figure 1.1 for a schematic overview of the chapters in this thesis). The remainder of this chapter introduces a conceptual framework for the empirical studies described in this thesis and the RE-PAIR (Relations and Emotions in Parent-Adolescent Interaction Research) study within which the data collection took place.
12 Chapter 1 Figure 1.1 Schematic overview of the theoretical framework and concepts examined in this thesis. MDD = Major depressive disorder. THE SIGNIFICANCE OF AFFILIATIVE BONDS As human beings, we are intrinsically social and have a deeply ingrained need to belong to others. This innate psychological drive to participate and invest in meaningful affiliative bonds is thought to be a heritage of our primal ancestors, who needed to cooperate in a group to gain access to food, shelter, and protection for attack (Allen, 2020). Although nowadays depending on others is no longer a case of life or death, the desire for social connection with others has remained and is reflected in our need to be (literally and figuratively) seen by others and its impact if this desire goes unanswered (Allen, 2020). From this perspective, the longing for social interactions is not merely a desire, but a fundamental need. Attachment theory proposes that the fundament of an individual’s ability to form and maintain social bonds with others is based on the attachment bond with one’s primary caregivers: The attachment figures (Ainsworth et al., 1978; Bowlby, 1969). This theory states that an infant’s early interactions with their attachment figure(s) shapes their attachment bond, and with that their ability to form and engage in other meaningful and satisfying relationships with those around them. One of the main reasons to think that this parent-child attachment bond is of paramount importance is that early positive experiences in the parent-child rearing context have a positive impact on how the socio-emotional pathways in the brain are wired and give a secure base from
1 13 General introduction which a child can explore the (social) world around them (Feldman, 2017; Schore, 2013). As such, the parent-child attachment bond is a foundation for future relationships into adulthood (e.g., romantic relationships, friendships) and a starting point for the development of a child’s social competences (Pratt et al., 2017). NEURAL SYSTEMS OF ATTACHMENT AND AFFILIATIVE BONDING Studies on neural signatures of the parent-child bond seem to agree on an “attachment network” in the brain (Abraham et al., 2018; Atzil et al., 2011; Barrett et al., 2012; Elmadih et al., 2016; Feldman, 2017; Kuo et al., 2012; Leibenluft et al., 2004; Lenzi et al., 2009; Shimon-Raz et al., 2021; Swain et al., 2014; Wan et al., 2014). In response to the sight of one’s own child (versus an unfamiliar child) parents typically show increased activation in neural networks supporting complex social functions that are important for parental caregiving, such as resonating with other’s mental states and emotions in the anterior insula, anterior cingulate cortex, inferior frontal gyrus, inferior parietal lobule, and supplementary motor area (i.e., embodied simulation network, including the affective empathy network) and social cognition, mental-state understanding, and social goal interpretation in the medial prefrontal cortex, temporoparietal junction, temporal pole, posterior cingulate gyrus, superior temporal sulcus (i.e., mentalizing network, including the cognitive empathy network) (Feldman, 2017). See Figure 1.2 for a schematic overview of this “attachment network”. Moreover, these brain regions have been consistently linked to subjective (self-report) and objective (behavioral observations) measures of parental caregiving and parentchild bonding. It is of note, however, that the lion’s share of these studies has been conducted in parents of infants and young children. Interestingly though, a recent study has found that these attachment-related patterns of activation were independent of a child’s age, representing a parent’s and child’s attachment relationship throughout life from infancy to adulthood (UlmerYaniv et al., 2021). Less is known about neural signatures of socio-emotional connectedness between a parent and a child during adolescence. This thesis therefore investigated neural signatures of two meaningful processes common within the parent-child relationship during adolescence: Socio-emotional connectedness of parents and adolescents when making eye contact with each other and parental empathic responses during the imagined suffering of their child.
14 Chapter 1 Figure 1.2 Schematic overview of brain regions involved in the “attachment network” (after Feldman (2017)), including the embodied simulation/affective empathy network (red) involved in resonating with others’ mental states and emotions and the mentalizing/cognitive empathy network (green) involved in social cognition, mental-state understanding, and social goal interpretation. ACC = Anterior cingulate cortex, AI = Anterior insula, dmPFC = Dorsomedial prefrontal cortex, IFG = Inferior frontal gyrus, IPL = Inferior parietal lobule, PCC = Posterior cingulate cortex, SMA = Supplementary motor area, STS = Superior temporal sulcus, TP = Temporal pole, TPJ = Temporoparietal junction, vmPFC = Ventromedial prefrontal gyrus. EYE CONTACT Eye contact is a social cue that initiates and regulates social interaction and facilitates the formation and maintenance of social ties between people (Emery, 2000; Hietanen, 2018). Although the attentional and cognitive processes related to eye contact have been extensively
1 15 General introduction studied in the literature, the affective component of eye contact is a road less explored (Hietanen (2018), for a review). Interestingly, it is this affective component of eye contact that is specifically associated with social bond formation and maintenance, and thus highly relevant to study in the context of socio-emotional connectedness between parents and adolescents. The importance of eye contact in social interaction has also been emphasized by the finding that receiving a direct gaze from others signals social inclusion and usually induces positive feelings in people, as it resonates with our intrinsic need to belong and literally be ‘seen’ (Hietanen, 2018; Kobayashi & Hashiya, 2011). It may also serve as a way to gain information about others’ mental states and conveys signals of empathy and social intimacy to others (Cowan, 2015; Cowan et al., 2014; Kleinke, 1986). Moreover, it is known that prolonged eye contact results in stronger affective responses and can elicit higher order socio-emotional processes, such as theory of mind processing and mentalizing, that are important for its communicative intent (Cavallo et al., 2015; Kuzmanovic et al., 2009). In addition to its importance in social bond formation in general, eye contact may also serve as an important form of communication within the parent-child bond. It constitutes one of the first acts of reciprocity between a parent and its newborn baby and is thought to be an important facilitator for a strong parent-child bond and a secure attachment (Robson, 1967). Moreover, it has been shown that our tendency to make eye contact is innately driven as 2-5 days old newborns already show a preference for eye contact versus an averted gaze and 4-months-old infants show enhanced neural processing of faces with a direct versus averted gaze (Farroni et al., 2002). Being able to get the attention of one’s parent by making eye contact enables infants to signal their physical and emotional needs for food and comfort of the parent. At the same time, the rewarding impact of positive affect in response to eye contact with their child is thought to reinforce sensitive caregiving behavior in parents towards the child (Robson, 1967). Since affective responses to eye contact seem to be an innately driven adaptation to our complex social surroundings (Kobayashi & Hashiya, 2011), it does not come as a surprise that this is also reflected in our neural responses. Most neuroimaging studies conducted on eye contact have focused on neural responses to the detection and recognition of a direct versus averted gaze of others, using short stimuli of <2 seconds. These studies have broadly distinguished two networks: A subcortical pathway (i.e., superior colliculi/periaqueductal grey, pulvinar nuclei and amygdala) for a ‘quick and dirty’ detection of gaze direction and a more reflective cortical pathway (i.e., fusiform gyrus, superior temporal sulcus, medial prefrontal cortex and orbitofrontal cortex) for the evaluation of eye contact (Hietanen, 2018; Senju & Johnson, 2009). Only a small number of studies have focused more specifically on the affective and affiliative responses to prolonged eye contact during interpersonal contact with others, using stimuli with a longer presentation duration. These studies investigated higher-order processes, i.e., theory of mind
16 Chapter 1 processing and mentalizing, that most likely come into play as the duration of eye contact increases (Cavallo et al., 2015; Kuzmanovic et al., 2009). These studies found that prolonged eye contact (i.e., 2-30 seconds) resulted in differential neural responses in orbitofrontal gyrus, inferior frontal gyrus, dorsomedial prefrontal cortex, paracingulate regions, anterior insula, premotor and supplementary motor area compared to short stimuli of <2 seconds. These brain regions are, amongst other things, involved in the preparation of a communicative response and the initiation of social interaction. To assess parents’ and adolescents’ responses to eye contact with one another, we designed a fMRI paradigm and compared these responses to eye contact with unknown others (i.e., an unfamiliar peer or adult). This allows for a better understanding of neural and affective processes in response to prolonged eye contact during warm and affectionate interactions between parents and adolescents of well-functioning families. Moreover, this will function as a solid baseline that helps to investigate potential alterations in these processes in situations in which parents and adolescents have difficulties to connect with each other. INTER-INDIVIDUAL DIFFERENCES IN CONNECTEDNESS Two inter-individual factors that are known to be associated with difficulties in social interactions and are found to have a negative impact on family dynamics, are childhood emotional maltreatment and depression. What these factors have in common is that they are linked to altered (more negative) cognitive schemas about others and the self, which may affect one’s ability to engage in interpersonal contact. As these processes might be strongly ingrained in one’s way of responding to social cues, it is of interest to examine whether parents with a history of childhood emotional maltreatment and depressed adolescents show altered responses to gazing into the eyes of their child or parent, respectively, and of unknown others. Childhood emotional maltreatment is common and includes situations in which parents fail to accurately perceive and appropriately respond to the emotional and psychological needs of their child. It encompasses both emotional abuse (i.e., verbal assaults and demeaning behaviors directed towards children by adults that are harmful for a child’s self-worth) and emotional neglect (i.e., caregivers’ irresponsibility or failure in satisfying children’s basic psychological needs for love, belonging, nurturance, and support) (Bernstein et al., 1994; Bernstein et al., 2003). Childhood emotional maltreatment can give rise to long-term negative consequences far into adulthood, including the development of negative cognitions about the self and others, possibly due to the perceived betrayal of trust during childhood by a primary caregiver (Baugh et al., 2019; Reyome, 2010; van Harmelen et al., 2010). People who have experienced childhood emotional maltreatment might on the one hand generalize distrust to others, believing that
1 17 General introduction everyone has bad intentions (maladaptive other-schemas), while on the other hand it may lead them to believe that they are unloved, worthless, or unwanted (maladaptive self-schemas) (Baugh et al., 2019; Gobin & Freyd, 2014). These beliefs put them at risk for the development of internalizing disorders, such as anxiety and depression, and can contribute to interpersonal difficulties and problems in affiliative bond formation and maintenance (Reyome, 2010; Riggs, 2010; Wright et al., 2009). Moreover, there is evidence for the intergenerational transmission of childhood emotional maltreatment, showing that having a history of childhood emotional maltreatment as a parent raises the risk of maltreating one’s own children (Lotto et al., 2023; Madigan et al., 2019). It is of note, however, that this relationship is far from deterministic in a way that people who have been maltreated as a child not always become a perpetrator of emotional maltreatment towards their own children (Madigan et al., 2019). Depression is common during adolescence. This is thought to be linked to the enhanced sensitivity to social evaluation during adolescence, which may make adolescents especially vulnerable to develop depression in response to negative social experiences (e.g., bullying, exclusion, and rejection) (Crone & Dahl, 2012; Dahl, 2004; Giedd & Rapoport, 2010; Hankin & Abramson, 2001; Wilson et al., 2015). Adolescent depression is characterized by difficulties in the social domain, including social isolation and dysfunctional interpersonal relationships, putting a strain on their relationship with others, including peers and parents (Babore et al., 2016; Branje et al., 2010; Heaven et al., 2004; Sheeber et al., 2001). The latter is also reflected in studies who found that depressed adolescents reported lower levels of relationship satisfaction with their parents compared to non-depressed adolescents, although it is unsure whether this is related to an altered perception due to their depressed state or to an actually worse relationship with their parents (Branje et al., 2010; Restifo & Bögels, 2009; Sheeber et al., 2001; Yap et al., 2014). PARENTAL EMPATHY Empathy can generally be defined as the capacity to share an emotional state with another individual, assess the reasons for the other’s state, and identify with the other by adopting his or her perspective (De Waal & Preston, 2017). Although the capacity to empathically respond to others is essential to the regulation of social interactions in general, it is thought to be evolved in the context of caregiving. Parental empathy is deemed fundamental for sensitive caregiving (Abraham et al., 2018; De Waal, 2008; Decety, 2011). As our social lives became increasingly complex across human evolution, caregiving behavior became more complex too. Consequently, human caregiving slowly transitioned from mainly protecting offspring from potential physical threats into preparing them for successfully navigating in our complex social worlds. Empathic parents provide more attuned care for their children, resulting in securely attached and stable
18 Chapter 1 parent-child bonds (Kochanska, 1997), which fosters a child’s socio-emotional development (Abraham et al., 2018; Manczak et al., 2018; Richaud et al., 2013; Soenens et al., 2007). The neural correlates of empathy have been extensively studied and broadly two neural systems can be distinguished. The core of empathic responses is the affective empathy network, including bilateral anterior insula (AI) and anterior mid-cingulate cortex (aMCC) (De Waal & Preston, 2017; Shamay-Tsoory, 2011). This network supports the vicarious experience of affect and thereby facilitates emotion contagion and affect sharing. It may help parents to appropriately “feel” the emotions and needs of their children, which could then promote carrying out adequate caregiving responses needed for sensitive parenting (Abraham et al., 2018; Ainsworth et al., 1978; Fan et al., 2011; Feldman, 2017; Turpyn, 2018). In addition, a more recently evolved cognitive empathy network has been identified that includes regions in temporal, parietal and prefrontal cortex (De Waal, 2008; De Waal & Preston, 2017; Decety, 2011; Decety & Jackson, 2004; Shamay-Tsoory et al., 2009; Zaki & Ochsner, 2012). More specifically, this network includes the dorsomedial prefrontal cortex (dmPFC), ventromedial prefrontal cortex (vmPFC), temporoparietal junction (TPJ), temporal pole, superior temporal sulcus, and frontopolar cortex (Abraham et al., 2018; Feldman, 2017; Shamay-Tsoory, 2011), and facilitates understanding of another’s point of view by making inferences of others’ mental states (Shamay-Tsoory, 2011). In the context of parenting, this cognitive empathy network may promote a better understanding of the feelings, actions, and intentions of the child (Abraham et al., 2018). As parental empathy is, in fact, an important pillar of the attachment bond between a parent and child, it is no surprise that there is extensive overlap between the neural correlates of the affective and cognitive empathy networks and the “attachment network” presented in Figure 1.2. Although parents’ empathic responses towards babies and young children have been studied extensively (Abraham et al., 2018; Atzil et al., 2011; Barrett et al., 2012; Elmadih et al., 2016; Kuo et al., 2012; Leibenluft et al., 2004; Lenzi et al., 2009; Wan et al., 2014), less is known about these responses when parenting an adolescent child. This is remarkable, as the increasing autonomy of adolescents and more time spend outside adult supervision creates situations where parents are not involved in. When a child, in turn, verbally shares their distress about an unpleasant situation (e.g., being excluded from a peer group) it might be more difficult for parents to imagine how their child would feel and might place higher demands on their sociocognitive capacities needed for an appropriate empathic response. One of the pillars of this thesis was to examine the neural and psychological signatures of parental empathic responses to the imagined suffering of their adolescent child. Moreover, we additionally investigated to what extent inter-individual differences in parental warmth are related to parents’ neural responses to their child’s suffering to examine whether these neural responses can serve as a marker for the parent-child bond.
1 19 General introduction Another facet of empathic behavior that is of interest to social interactions between people, both within and outside the parent-child bond, is the ability of people to accurately infer others’ feelings, also referred to as empathic accuracy (Ickes & Hodges, 2013; Zaki et al., 2008; Zaki et al., 2009). Several studies have emphasized that the eye region is an important source of social cues that contribute to one’s ability to be empathically accurate about others’ internal state (Baron-Cohen et al., 1997; Buchan et al., 2007; Eisenbarth & Alpers, 2011; Hall et al., 2010; Zaki et al., 2009). However, the lion’s share of these studies included paradigms in which empathic accuracy was assessed in response to static pictures of others, which limits generalizability to real life social situations. A hand full of studies that did make use of close-to-real life dynamic video stimuli found a positive link between people’s trait empathy levels and the amount of eye contact they made with others, especially under emotionally valenced circumstances (Cowan et al., 2014; Martínez-Velázquez et al., 2020). However, these studies did not include whether gazing into the eyes contributes also to being more empathically accurate about others’ feelings. To bridge this gap, we adapted an already existing empathic accuracy task by simultaneously measuring participants gaze using eye tracking. The task includes emotionally valenced target stories, including both visual and verbal (speech) informational cues, closely mimicking real life social settings. As little is known about the role of eye contact in empathic accuracy this study focused on this relationship in adults towards unknown other adults. THE RE-PAIR STUDY The empirical studies in this thesis take place in the context of the RE-PAIR study: “Relations and Emotions in Parent-Adolescent Interaction Research”. This study uses a multi-method and multi-informant approach to examine the relation between parent-adolescent interactions and adolescent well-being by comparing adolescents with a current diagnosis of a major depressive disorder (MDD) or dysthymia and their parents to adolescents without psychopathology and their parents (i.e., healthy control families). Moreover, we included both mothers and fathers in the study, which allows for the assessment of potential gender differences in the socioemotional connection between parents and their adolescent child. The RE-PAIR study consists of four parts: An online questionnaire battery, a research day in the lab, two weeks of ecological momentary assessment (EMA), and an MRI scan session in which we focus on concepts relevant for the parent-child relationship during adolescence and adolescent depression (e.g., parental empathy, eye contact, responses to feedback of parents, peers and unfamiliar others, and autobiographical memory processing). See Figure 1.3 for an overview of the RE-PAIR study and the specific parts used to answer the research questions in the present thesis.
20 Chapter 1 Figure 1.3 Schematic overview of the RE-PAIR study and specific tasks that have been used to answer the research questions in the present thesis. EMA = Ecological momentary assessment, fMRI = Functional magnetic resonance imaging. OUTLINE OF THIS THESIS The research described in this thesis investigated the neural and affective signatures of connectedness between parents and adolescents, which was operationalized by the assessment of parents’ and adolescents’ responses to making eye contact with each other and parental empathy. To assess this, we developed two novel fMRI paradigms to study the neural correlates of these processes in the brains of parents and adolescents. In addition, we examined the uniqueness of these responses to the parent-child bond by comparing these responses to how parents and adolescents respond to unknown others in similar situations. We examined these processes first in parent-adolescent dyads in well-functioning families in order to gain more insight in these processes under ‘normal’ conditions. In addition, we studied the impact of a history of childhood emotional maltreatment in parents and adolescent depression on parents’ and adolescents’ neural and affective responses to their mutual connectedness. Chapter 2 examined parents’ neural and affective responses to prolonged eye contact with one’s own child versus unfamiliar others. Chapter 3 examined the impact of a history of childhood emotional maltreatment in parents on their neural and affective responses to gazing into their own and others’ eyes. Chapter 4 investigated adolescents’ neural and affective responses
1 21 General introduction when making prolonged eye contact with their parent and unknown others. In addition, differences in these responses between depressed and non-depressed adolescents were examined. Chapter 5 examined parents’ empathic responses to the imagined suffering of their adolescent child. In addition, it was examined whether these empathic responses may function as a marker for the parent-child bond by relating these responses to measures of parental care as reported by the adolescent child. Chapter 6 examined the contributing role of eye contact to parents’ empathic accuracy and to their individual state and trait levels of perspective taking and empathic concern towards unknown others in an emotionally valenced social setting. Lastly, Chapter 7 summarized the findings of this thesis and discussed them in the context of connectedness between a parent and adolescent child, the uniqueness of the findings to the parent-adolescent bond, and whether a history of childhood emotional maltreatment in parents and adolescent depression are associated with altered responses to connectedness between parents and adolescents and with unknown others.
Chapter 2 Chapter 2 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others. Chapter 2 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others Published as: Wever, M.C.M., van Houtum, L.A.E.M., Janssen, L.H.C., Wentholt, W.G.M., Spruit, I.M., Tollenaar, M.S., Will, G-J., & Elzinga, B.M. (2022). Neural and Affective Responses to Prolonged Eye Contact with One’s Own Adolescent Child and Unfamiliar Others. Neuroimage, 119463. https://doi.org/10.1016/j.neuroimage.2022.119463. Link to preregistration prior to data analyses: https://osf.io/54nky/
24 Chapter 2 ABSTRACT Eye contact is crucial for the formation and maintenance of social relationships, and plays a key role in facilitating a strong parent-child bond. However, the precise neural and affective mechanisms through which eye contact impacts on parent-child relationships remain elusive. We introduce a task to assess parents’ neural and affective responses to prolonged direct and averted gaze coming from their own child, and an unfamiliar child and adult. While in the scanner, 79 parents (n = 44 mothers and n = 35 fathers) were presented with prolonged (16-38 s) videos of their own child, an unfamiliar child, an unfamiliar adult, and themselves (i.e., targets), facing the camera with a direct or an averted gaze. We measured BOLD-responses and tracked parents’ eye movements during the videos and asked them to report on their mood and feelings of connectedness with the targets after each video. Parents reported improved mood and increased feelings of connectedness after prolonged exposure to direct versus averted gaze and these effects were amplified for unfamiliar targets compared to their own child, due to high affect and connectedness ratings after videos of their own child. Neuroimaging results showed that the sight of one’s own child was associated with increased activity in middle occipital gyrus, fusiform gyrus and inferior frontal gyrus relative to seeing an unfamiliar child or adult. While we found no robust evidence of specific neural correlates of eye contact (i.e., contrast direct > averted gaze), an exploratory parametric analysis showed that dorsomedial prefrontal cortex (dmPFC) activity increased linearly with duration of eye contact (collapsed across all “other” targets). Eye contact-related dmPFC activity correlated positively with increases in feelings of connectedness, suggesting that this region may drive feelings of connectedness during prolonged eye contact with others. These results underline the importance of prolonged eye contact for affiliative processes and provide first insights into its neural correlates. This may pave the way for new research in individuals or pairs in whom affiliative processes are disrupted. Keywords: Eye contact; Gaze direction; Mentalizing; Parenting; Familiarity; fMRI
2 25 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others INTRODUCTION Humans are hard-wired to connect with others and an important non-verbal strategy to form and maintain strong social ties with other humans is by making eye contact (Emery, 2000; Hietanen, 2018; Kellerman et al., 1989). Receiving a direct gaze induces positive feelings and signals social inclusion, which fulfills our intrinsic need to belong, and to be literally ‘seen’ (Hietanen et al., 2018; Hietanen et al., 2020; Kiilavuori et al., 2021; Kleinke, 1986). Eye contact constitutes one of the first acts of reciprocity between a parent and a child (Robson, 1967), and is thought to be an important facilitator for a strong parent-child bond and secure attachment. Moreover, positive affective responses of parents to eye contact with their own child are thought to reinforce sensitive caregiving behavior (Robson, 1967). To date, we know remarkably little about what exactly happens in the parental brain when parents make eye contact with their child. Nor do we know whether these responses are unique to the parent-child context or generalize to eye contact with unfamiliar others. A better understanding of the role of eye contact in social interaction might generate new insights for those having difficulties connecting with others via eye contact on a social and emotional level, both within and outside the parent-child context, and pave the way for interventions. Therefore, we examined neural and affective processes in parents when they make prolonged eye contact with their own child. We contrast personalized videos of their own child against videos of an unfamiliar child or adult and employed a multimethod approach including self-reports of affect, functional magnetic resonance imaging (fMRI), and eye tracking. It is known that people show specific (neural) response to faces of personally familiar compared to unfamiliar others (Petrowski et al., 2019; Ramon & Gobbini, 2018; Taylor et al., 2009), and such studies have often been conducted within the parent-child context (Abraham et al., 2018; Atzil et al., 2011; Barrett et al., 2012; Elmadih et al., 2016; Kuo et al., 2012; Lenzi et al., 2009; Wan et al., 2014). In response to the sight of their own child (versus unfamiliar children) parents typically show increased activation in neural networks supporting complex social functions that are important for parental caregiving, such as theory of mind, empathy, and interpersonal closeness/attachment (i.e., medial prefrontal cortex (MPFC), temporal parietal junction (TPJ), anterior insula, anterior cingulate cortex, amygdala, and inferior frontal gyrus (IFG) (Abraham et al., 2018; Atzil et al., 2011; Shimon-Raz et al., 2021). Moreover, these brain regions have been consistently linked to parental caregiving and attachment to the child and activations were independent of a child’s age, representing one’s attachment relationship throughout life from infancy to adulthood (Shimon-Raz et al., 2021; Ulmer-Yaniv et al., 2021). In addition to neuroimaging studies on the processing of faces as a whole, there is a vast amount of research on neural responses to direct (versus averted) gaze of unfamiliar individuals. These studies have broadly distinguished two networks: A subcortical pathway (i.e., superior colliculi/periaqueductal grey, pulvinar nuclei and amygdala) for a ‘quick and dirty’ detection of
26 Chapter 2 gaze direction and a more reflective cortical pathway (i.e., fusiform gyrus, superior temporal sulcus, MPFC and orbitofrontal cortex) for the evaluation of eye contact, i.e. theory of mind and mentalizing (Hietanen, 2018; Senju & Johnson, 2009). However, these pathways are based on studies generally using stimuli with a short duration (< 2 seconds) and with a focus on the effect of gaze direction on facial recognition processes, while the neural correlates of prolonged eye contact are understudied. This is striking as the affiliative role of eye contact in interpersonal contact with others most likely comes into play as the duration of eye contact increases. For example, behavioral studies have shown that a prolonged presentation duration of dynamic face stimuli induces greater emotional engagement (Cowan et al., 2014; Regenbogen et al., 2012) and more favorable judgements from receiver to sender (Argyle et al., 1974; Brooks et al., 1986; Kuzmanovic et al., 2009; Montgomery et al., 1998). Prolonged exposure is also thought to more strongly engage higher-order cognitive processes related to the evaluation of eye contact, such as mentalizing in order to infer others’ thoughts and feelings (Eskritt & Lee, 2007; Kuzmanovic et al., 2009). To date, only two studies focused on neural responses to prolonged eye contact. Kuzmanovic et al. (2009) examined the impact of varied gaze durations (i.e., 1, 2.5, and 4 s) on participants’ neural responses to direct and averted gaze and found that increased duration of direct gaze resulted in differential neural responses in MPFC, including orbitofrontal and paracingulate regions. In addition, Cavallo et al. (2015) examined participants’ neural responses to prolonged eye contact using stimuli of 15-30 s. They reported differential neural activation in IFG, anterior insula, pre-motor and supplementary motor area in response to direct versus averted gaze (i.e., gaze direction) of others. These brain regions are involved in the preparation of a communicative response, also referred to as a ‘readiness potential’ for the initiation of a social interaction (Cavallo et al., 2015; Gallagher, 2014; Pfeiffer et al., 2013; Saito et al., 2010). In addition, Cavallo et al. (2015) found the dorsomedial prefrontal cortex (dmPFC) to be specifically activated when participants reciprocated the direct gaze of the target to establish a mutual gaze. To capture neural correlates of positive affect and feelings of connectedness elicited by prolonged eye contact, we developed a new fMRI paradigm to examine parents’ neural and affective responses to direct versus averted gaze stimuli with a prolonged presentation duration of 16-38 s. In this task, parents (n = 79, 44 mothers and 35 fathers) of adolescent children (aged between 12-18 years) made eye contact with their own child versus an unfamiliar child and adult. More specifically, we examined whether parents report a better mood and enhanced feelings of connectedness (affective responses) and show enhanced neural responses while making eye contact with others, and whether this is modulated by the person with whom they made eye contact in the videos (i.e., own child, an unfamiliar child or unfamiliar adult). In addition, we examined to what extent parents gazed towards the eye region of the targets during the direct gaze (versus averted gaze) conditions and whether these responses are modulated by the identity of the targets. As adolescence is a crucial period for social development and a good
2 27 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others parent-child relationship is one of the most important factors supporting adolescents’ wellbeing (Steinberg & Silk, 2002), it is of great importance to not only examine parental responses in parents of babies or young infants, but also during adolescence. In addition, adolescents start to become more autonomous in their relationship with their parents and eye contact might substitute physical contact between a parent and child that is more pronounced during infancy and may be less appreciated during adolescence (Montemayor, 1983; Montemayor, 1986; Steinberg & Silk, 2002). All study measures, hypotheses, and analyses were preregistered at Open Science Framework prior to data analyses (https://osf.io/54nky/). Based on prior studies on parent-child bonding (Abraham et al., 2018; Atzil et al., 2011; Barrett et al., 2012; Elmadih et al., 2016; Kuo et al., 2012; Lenzi et al., 2009; Wan et al., 2014), we expected that parents report a better mood and enhanced feelings of connectedness after making eye contact with others (compared to an averted gaze). We also expected that differences in mood and feelings of connectedness between direct and averted gaze were most pronounced in response to videos of the own child versus an unfamiliar child or adult. At the neural level, we expected that parents generally show increased neural responses in the subcortical and cortical pathway of face processing in response to direct versus averted gaze. We hypothesized that parents would show enhanced responses in neural networks supporting social cognition, such as theory of mind (i.e., MPFC, TPJ) and salience processing (i.e., insula, ACC, amygdala) in response to videos of their own child versus an unfamiliar child or adult. Based on prior work of Leibenluft et al. (2004), we expected enhanced responses at the neural, but not at the affective level, to an unfamiliar child versus adult. Lastly, we explored an interaction between gaze direction (i.e., direct versus averted gaze) and target person (i.e., with whom parents made eye contact) to examine whether a direct gaze facilitates parents’ responses to their own child versus others. We expected that parents would gaze more towards the eyes of targets during direct versus averted gaze videos. Given that no studies have examined whether gazing to the eyes of others is modulated by personal familiarity or interpersonal closeness (i.e., own child versus unfamiliar targets), we formulated no concrete hypotheses regarding this question. METHOD Participants Data were collected in the context of the RE-PAIR study: “Relations and Emotions in ParentAdolescent Interaction Research”. The RE-PAIR study uses a multi-method approach to examine the relation between parent-child interactions and adolescent depression by comparing families with an adolescent with a current diagnosis of a major depressive disorder (MDD) or dysthymia to families with an adolescent without psychopathology. Families were included in the study if the
28 Chapter 2 adolescent and at least one of the parents/caregivers were willing to participate in the study and had a good command of the Dutch language. Families were explicitly asked to participate with both parents/caregivers, if possible, although this was no requirement for inclusion. Adolescents were required to be aged between 11 and 17 years at study inclusion and to live with at least one of their parents/caregivers. Families with an adolescent without psychopathology were included in the study if they were not diagnosed with a (neuro)psychiatric disorder in the two years leading up to the study and had no lifetime diagnosis of MDD or dysthymia. Families with an adolescent with MDD/dysthymia were included in the study if the adolescent met criteria for one of these current primary diagnoses, verified with the Kiddie-Schedule for Affective Disorders and Schizophrenia Present and Lifetime version (K-SADS; Kaufman et al. (1996)). Families could not participate if the adolescent met criteria for a primary diagnosis of a current (neuro)psychiatric disorder other than MDD or dysthymia, or a comorbid psychosis, substance use disorder or mental retardation. Additionally, exclusion criteria for the functional magnetic resonance imaging (fMRI) part of the study were incompatibilities with MRI scanning (e.g., metal implants, pregnancy). The present study focused on fMRI data collected during the scan session both from parents of adolescents with and without psychopathology in this larger study. Eighty-five parents participated in this study. Six parents were excluded from data analyses due to brain abnormalities (n = 1), ending the scan session due to symptoms of sleep apnea (n = 1), incomplete datasets (n = 3), and an a posteriori clinical diagnosis of the adolescent other than a primary diagnosis of MDD or dysthymia (n = 1). This resulted in a final sample of 79 parents of adolescents, including 44 mothers (Mage = 48.03 years, SDage = 3.89) and 35 fathers (Mage = 52.19 years, SDage = 4.47). See Table 2.1 for details on sample demographics. The study was approved by the medical ethical committee of the Leiden University Medical Centre (LUMC) (P17.241) and was performed in accordance with the declaration of Helsinki and the Dutch Medical Research Involving Human Subjects Act (WMO).
2 29 Neural and affective responses to prolonged eye contact with one’s own adolescent child and unfamiliar others Table 2.1 Demographic characteristics All parents Mothers Fathers Mothers vs. fathers1 Mean (SD) / n (%) (n = 79) (n = 44) (n = 35) t / χ2 p Age parent, years 49.87 (4.62) 48.03 (3.89) 52.19 (4.47) 4.43 <.001 Age adolescent, years 16.44 (4.23) 17.19 (5.42) 15.51 (1.51) 0.77 .082 Gender adolescent Boys, n (%) 25 (31.6) 13 (29.5) 12 (34.3) 0.04 .842 Girls, n (%) 54 (68.4) 31 (70.5) 23 (65.7) 1.19 .276 Adolescent depression severity2 8.11 (7.04) 7.07 (6.65) 9.43 (7.40) 1.49 .140 Education of parents Vocational training, n (%) 18 (22.8) 11 (25.0) 7 (20.0) 0.89 .346 Higher education, n (%) 61 (77.2) 33 (75.0) 28 (80.0) 0.41 .522 Note. SD, Standard deviation. 1 p-values were obtained using independent samples t-tests or Chi-square comparisons between mothers and fathers. 2 Assessed with the Patient Health Questionnaire (PHQ-9; Kroenke et al. (2001)) prior to the first visit in the lab. Procedure Families with an adolescent without psychopathology were recruited via public advertisements and (online) social media, including Facebook and advertisement in the monthly magazine of the Royal Dutch Touring Club (ANWB). Families with an adolescent with MDD/dysthymia were recruited via mental health facilities. Parents and adolescents were briefed about the study and underwent a comprehensive telephone screening during which family circumstances and informed consent were discussed and adolescents were pre-screened for (a history of) psychiatric disorders. Families were invited for two appointments: An assessment day in the lab and an MRI session on a separate day. Prior to the first appointment parents were asked to fill out an online questionnaire battery including demographics and clinical and cognitive measures. During the first appointment, families performed parent-adolescent interaction tasks and filled out additional questionnaires, and parents were screened on current psychopathology with the Mini International Neuropsychiatric Interview (see Supplement S2.1). During the second appointment, parents underwent an MRI scan at the LUMC in Leiden, the Netherlands. Prior to the scan, parents filled out a set of questionnaires, received instructions about the MRI tasks, and performed some practice trials. Parents performed three tasks in the MRI scanner: The eye contact task as described below, a parental empathy task (Wever et al., 2021), and a vicarious social feedback task (van Houtum et al., 2021). Upon completion of the MRI scans, parents were fully debriefed about the goals of the study and received a monetary compensation and travel allowance. Parents provided written informed consent for each individual testing day. The median of days between the first and second appointment was 37 and ranged between 7 and 265 days.
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