Maternal Depression and Adolescent Attention to Self- Or Other-Directed Emotional Faces

MATERNAL DEPRESSION AND ADOLESCENT ATTENTION TO SELF- OR OTHER-DIRECTED EMOTIONAL FACES

SAMUEL BLOOM SEIDMAN

Submitted in partial fulfillment for the requirements

For the degree of Master of Arts

Department of Psychological Sciences

CASE WESTERN RESERVE UNIVERSITY

August, 2020

CASE WESTERN RESERVE UNIVERSITY

SCHOOL OF GRADUATE STUDIES

We hereby approve the thesis of

Samuel Bloom Seidman

Candidate for the degree of Master of Arts*.

Committee Chair

Arin M. Connell, Ph.D.

Committee Member

Anastasia Dimitropoulos, Ph.D.

Committee Member

Amy Przeworski, Ph.D.

Date of Defense

April 27, 2020

*We also certify that written approval has been obtained for any proprietary material

contained therein.

Table of Contents

List of Tables 5

List of Figures 6

Acknowledgement 7

Abstract 8

Introduction 9

Maternal Depression & Child Risk 9

Attention Biases in Depression 11

Emotion Faces & Gaze Orientation 13

Neural Processing of Emotion Faces 15

N200 15

N400 15

Late Positive Potential 16

The Present Study 17

Methods 18

Participants 18

Measures 19

Procedures 21

Analysis Plan 22

Results 22

Discussion 25

Limitations and Future Directions 30 4

Appendix 32

Face viewing task

Center for Epidemiological Studies – Depression Scale

Child Depression Inventory

Tables 37

Figures 41

References 45 5

List of Tables

Table 1. Means for demographic characteristics of the youths and their parents. 37

Table 2. Bivariate Correlations. 38

Table 3. Repeated Measures ANOVAs with maternal depression history as a between subjects variable. 39

Table 4. Descriptive Statistics for N200, N400, & LPP Amplitudes. 40

List of Figures

Figure 1. Grand averaged ERPs for straight and averted faces across emotions and risk groups (high vs low risk). 41

Figure 2. N200 amplitude for averted vs. forward oriented faces in high risk (maternal depression history) and low risk (no maternal depression history) youth averaged across electrodes 42

Figure 3. N400 amplitude for averted vs. forward oriented faces in high risk (maternal depression history) and low risk (no maternal depression history) youth averaged across electrodes 43

Figure 4. LPP amplitude for averted vs. forward oriented faces in high risk (maternal depression history) and low risk (no maternal depression history) youth averaged across electrodes Fz, Cz, and Pz. 44

Acknowledgements

I would like to express my appreciation to my research adviser, Arin M. Connell,

Ph.D., for his contribution towards and support of this research project. I would like to thank the members of the Relationship, Emotions, and Family (REF) lab and the participants in the Family Relationships and Emotions in Youth (FREY) study. Finally, I would also like to thank my committee members, Anastasia Dimitropoulos, Ph.D. and

Amy Przeworski, Ph.D. for their participation and consideration.

Maternal Depression And Adolescent Attention To Self- Or Other-Directed Emotional

Faces

Abstract

SAMUEL BLOOM SEIDMAN

Maternal depression history represents a significant risk factor for developing psychopathology in children, altered emotional responding may represent a central risk pathway. In particular, facial orientation and gaze direction may be altered in high-risk youth. The present study utilized a task with altered face dimensions in order to measure differences in response to forward and averted emotion faces in relation to familial risk for depression. Three Event-Related Potential (ERP) components were examined: the

N200, N400, and Late Positive Potential (LPP) in a sample of youth based on maternal depression history (N = 56). Results showed low-risk youth exhibited more negative

N200 and N400 amplitudes for straight versus averted faces, while high-risk youth showed undifferentiated responses to face orientation. For LPP amplitudes, low-risk youth exhibited significantly more positive LPP amplitudes than high-risk youth, but only for averted faces. Results suggest differential sensitivity to the personal-relevance of emotional stimuli.

Introduction

A substantial literature has documented that the risk for developing psychopathology, including both internalizing and externalizing disorders, is higher for children of individuals with a history of depression (e.g. Beardslee, Gladstone, &

O’Conner, 2011; Goodman et al., 2011; Hammen, Hazel, Brennan, & Najman, 2012;

Klein, Lewinsohn, Rohde, Seeley, & Olino, 2005). For instance, maternal depression is associated with lifetime rates of depression in offspring from 20% to 41% (Goodman,

2007) compared to 13.3% in the general population (Substance Abuse and Mental Health

Services Administration, 2018). Furthermore, compared to peers with no parental depression history, youth with a family history of depression tend to have a greater number of mood disorder episodes, at an earlier age of onset, and experience greater functional impairment (Hammen, Burge, Burney, & Adrian, 1990; Hammen, Shih,

Altman, & Brennan, 2003; Weissman et al., 2006).

Maternal Depression & Child Risk

In particular, maternal depression (as opposed to paternal depression) has been associated with heightened risk for not only depression in youth but also other internalizing disorders and externalizing disorders. For example, in their meta-analysis of the literature Connell & Goodman (2002) found that while externalizing symptoms in childhood were related to both mothers and father’s psychopathology, child internalizing symptoms were more closely related to psychopathology in mothers. And in particular, maternal depression was uniquely related to development of internalizing disorders in children. The authors explain the difference as likely the result of complex mix interactions between biological and parenting factors. Further, the impact of maternal 10 depression on risk for internalizing disorders is heightened in mother-daughter dyads

(compared with mother-son dyads) (Goodman, et al 2011). Therefore, the present study seeks to explore the unique relationship of maternal depression on the development of internalizing disorders in daughters.

As noted, maternal depression history is a complex risk factor for youths with multiple pathways of potential transmission. Developmental models highlight the risk conferred from parents with a history of depression through a combination of inherited genes, innate neuroregulatory dysfunction, parenting style, and unique stressful life events (Goodman & Gotlib, 1999; Goodman, 2007). In this model proposed by

Goodman, & Gotlib, youth inherit genes from their depressed parents that leave biological systems vulnerable or otherwise confer personality traits associated with vulnerability. Additionally, neuroregulatory dysfunctions (developed through genetics or prenatal experiences) leave the youth more vulnerable to stress, negative emotions, or behavioral inhibition. In the context of the parent child dyad, parenting and modeling of negative cognitive, behavioral, and affective styles would be emulated by the child.

Finally, stressful life events, filtered through the inherited or learned negative affectivity would leave the youth vulnerable to respond maladaptively to stress. The model proposes an interactive effect of these biological and social influences which produce vulnerabilities for developing psychopathology.

Neuroregulatory dysfunction in particular has received interest and support across studies. Indeed, studies have demonstrated that depression reported during pregnancy and postnatally have been associated with disruptions in typical pregnancies such as low-birth weight (Accortt, Cheadle, and Schetter 2015), motor development (Nasreen, Kabir, 11

Forsell, & Edhborg 2013), as well as alterations in functioning across biological systems

(e.g. HPA axis, autonomic nervous system; Brennan, et al 2008; Buthmann, et al 2019).

For instance, Brennan and colleagues (2008) found that prenatal exposure to maternal depression was associated with higher cortisol reactivity in infants. Moreover, maternal depression during pregnancy has been associated with alterations in hippocampal and amygdala volume in offspring (Pulli, et al 2018). Such exposures have also been associated with early-life socioemotional, temperamental, and behavioral development

(Madigan, et al 2018). Therefore, it is likely that effects of maternal depression impact the course of typical neurodevelopment, through direct interference on brain development and related biological systems. These neuroregulatory dysfunctions may then manifest as affect biases (e.g. blunted positive processing) increasing risk for developing psychopathology.

Attention Biases & Depression

One important potential pathway of disorder transmission is the influence of parental depression on children’s understanding and perceptions of emotional expressions in other people (Belsky & de Haan 2011). Youth’s perceptions of others’ emotions are shaped in the context of close family relationships and based on the quality of the family environment (including parental behaviors and emotional responses; e.g. Chang,

Schwartz, Dodge, & McBride-Chang, 2003; Eisenberg et al., 1999). In particular, children in higher-risk environments may learn to attend specifically to emotional signals of potential threat, which may facilitate efforts to keep safe, although much of this work has focused on child maltreatment (e.g. Shackman, Fries, & Pollak, 2008). Further, alterations in responding to affective-stimuli have been identified as potential 12 mechanisms of depression onset and maintenance (Disner, Beevers, Haigh, & Beck,

2011), and as a vulnerability marker for depression in children of depressed parents

(Kujawa et al., 2011). These attention biases may develop as a consequence of youth’s perceptions of threat from their parent’s negative emotions (Connell, Danzo, Magee, &

Uhlman 2019). For instance, youth may become sensitive to signs of parental negative affect, which may signal potential threat to their well-being, facilitating avoidance of situations as an adaptive response to threat. Such attention biases for affective stimuli have been identified as a vulnerability marker for depression in children of depressed parents (Kujawa et al., 2011).

However, the nature of affective processing alterations related to depression risk remains unclear (Gibb, Pollack, Hajcak, & Owens, 2016). Proposed patterns range from diminished responding to positive emotions to heightened responding to negative emotions. The positive attenuation hypothesis argues that diminished responding to positive emotions (e.g. anhedonia) is a potential specific marker of depression (Clark &

Watson, 1991). Such patterns have been found across methods of inquiry including cognitive, neural, and genetic domains (Bogdan, Nikolova, & Pizzagalli, 2013). In contrast, the negative attenuation hypothesis holds that depression is best characterized by heightened negative cognitions and biases in information processing toward negative stimuli (Ingram, 1984). In line with this possibility, several studies have found that depression is associated with enhanced responding to sad (compared to happy or neutral) faces, suggesting that heightened responsivity to sad faces may represent a specific biomarker of depression-risk (Bistricky, Atchley, Ingram, & O’Hare, 2014). However, a growing literature suggests that depression risk may be related to a lack of discriminated 13 responding, more generally (i.e. dampened or non-discriminated responding to positive, negative, and neutral stimuli). This theory has been articulated most strongly as the

Emotion Context Insensitivity (ECI) theory, which proposes depression as an evolutionarily developed state of general withdrawal as a functional response to environments in which continued activity would be dangerous or futile (Rottenberg,

Gross, & Gotlib 2005). Indeed, ECI theory characterizes depression as a motivational state associated with disengagement from the environment, and has received support across measurement modalities (self-report, psychophysiological, etc; Bylsma, Morris, &

Rottenberg, 2008; Ellis, Beevers, & Wells, 2009). Given the range of findings in the literature, additional research is needed on factors that affect response alterations in relation to depression-risk in youth, in order to clarify conditions under which emotional response alterations may be heightened.

Emotion faces and gaze orientation

Given that faces convey a great deal of social information, efficient and accurate facial processing is crucial for adaptive social functioning (e.g. Conty, N’Diaye, Tijus, &

George, 2007). As discussed, there is evidence that high-risk family environments are associated with alterations in patterns of youth responding to affective stimuli, particularly human faces (including bias towards salient emotions, such as anger, fear, or sadness; Kujawa, et al 2011) although the precise nature of this bias is unclear (Gibb,

Pollack, Hajcak, & Owens, 2016). Similarly, ambiguous or ostensibly-neutral faces are often interpreted as hostile in clinical populations of youth, including those with internalizing or externalizing problems (Kelly, Maratos, Lipka, & Croker, 2016), and youth whose mothers have a history of depression (Connell et al., 2019), suggesting the 14 importance of fine-grained examination of the processing of facial emotions in relation to risk for psychopathology.

Moreover, neural processing of faces appears sensitive to features of facial stimuli, including facial orientation and gaze direction (Itier & Batty, 2009; McCrackin &

Itier, 2019), which offer crucial information regarding self-relevance that may guide affective processing (Adams & Kleck, 2005). Facial emotions directed towards an individual heighten motivational salience by conveying greater personal-relevance, compared to emotions directed away (Hamilton, 2016). For example, youth may interpret an angry or sad face directed at them as communicating more personal threat than an identical face directed elsewhere in the environment. Variations in face and gaze orientation have been shown to elicit distinct neural response patterns. Several studies have found enhanced N200 amplitudes (a face-sensitive ERP component detailed below) to direct-gaze compared to averted-gaze faces, suggesting more attention and processing resources devoted to these more personally-relevant faces (e.g. McCarthy et al, 1999;

Conty et al., 2007).

Furthermore, Bublatzky and colleagues (2017) found that angry faces directed toward participants elicited a more pronounced neural response than angry faces directed away from participants. Specifically, angry faces directed at participants resulted in a more pronounced neural response compared to neutral direct faces; they also found that angry faces directed at and toward participants elicited a more pronounced neural response than angry faces directed away from participants. Importantly, gaze direction has also been show to facilitate the communication of approach (e.g. joy and anger) and avoidance (e.g. fear and sadness) emotions (Adams & Kleck, 2003). Thus, gaze 15 orientation may communicate the potential self-relevance, or irrelevance, of incoming social and threatening information from emotions. To date, variations in facial-orientation or gaze direction do not appear to have been examined in relation to depression-risk.

Neural Processing of Emotion Faces

One promising avenue for enhancing our understanding of facial emotion processing is through the assessment of Event-Related Potentials (ERP), given their high temporal precision (e.g. Proudfit, Bress, Foti, Kujawa, & Klein, 2015; Schupp, Flaisch,

Stockburger, & Junghöfer, 2006). The current study examined three ERP components that have been associated with various aspects of human face processing, particularly their affective dimensions: the N200, N400, and Late Positive Potential (LPP). The N200 is a negative going ERP typically occurring at around 150-200ms post-stimulus onset.

N200 amplitudes appear to reflect early structural encoding of faces (Eimer, 2000a,

2000b) and the N200 has been shown to be sensitive to face direction and orientation, as well as eye direction (Conty et al., 2007; Itier, Latinus, & Taylor, 2006). For example,

Bublatzky et al (2017) observed a more pronounced N200 for faces directed at participants than faces directed away from them, suggesting that N200 reflects the motivational relevance of facial stimuli. Further, evidence suggests altered N200 responding to faces in youths with mood disorders: typically seen as an attenuated N200 amplitude to emotional faces relative to healthy youths (Grunewald et al., 2015; Tso et al., 2017).

The N400 is a negative going component occurring approximately 400ms following stimulus onset. In face-processing tasks, the N400 has been interpreted as representing higher-order processing of facial emotions, including accessing knowledge 16 about emotional displays and conscious evaluation of the semantic “meaning” of facial emotions (e.g. Olivares, et al, 2015; Paulmann & Pell, 2009). More negative N400 amplitudes have been observed for negative versus happy or neutral faces (Pegna, Landis,

& Khateb, 2008) or idiosyncratic expressions (e.g. grimace, compared to more prototypical positive or negative emotional displays), suggesting that greater processing resources may be required for accurate responding (Paulmann & Pell, 2009). Depression- related findings for the N400 have been mixed, with several studies finding no depression-related alterations of the N400 in responding to emotional words (e.g. Klump, et al, 2010). Others have found results in line with ECI theory. For instance, Dietrich and colleagues (2000) found that while healthy participants exhibited enhanced N400 amplitudes to negative words, depressed participants exhibited non-discriminated N400 responses across emotional word categories. Given that the N400 has classically been studied in response to incongruent or unexpected stimuli, this lack of discriminated N400 responding in depressed participants was interpreted as suggesting that negative emotional words were congruent with depressive mood states for depressed, but not healthy, participants. Emotional N400 alterations do not appear to have been examined in relation to familial risk for depression, to date.

Finally, the LPP is a positive going component occurring at around 500-800ms post-stimulus onset that has been associated with attention to and appraisal of emotional stimuli (Cuthbert, et al, 2000). For instance, it has been noted as particularly subject to modulation through the emotional content of the stimuli, the individual’s interpretations of the emotional stimuli, and the relevance of the stimuli to the subject (Pastor et al.,

2008; Schupp et al., 2000; Schupp, et al., 2006; Schupp, Flaisch, Stockburger, & 17

Junghöfer, 2004). The LPP has also been shown to be sensitive to visually or verbally presented emotional stimuli (Schacht & Sommer, 2009), to the recall of self-relevant emotional information (Auerbach, et al 2015), and to emotional faces (Schupp, et al

2004). Of particular relevance to the present study, the LPP has been noted as a marker of depression-risk in adolescence (Dennis & Hajcak 2009; Hajcak & Dennis, 2009). While healthy populations typically exhibit a more positive LPP response to emotional versus neutral stimuli, a lack of discriminated LPP responses to emotional versus neutral stimuli has been observed in both depressed youths, and youth at high familial risk for depression (e.g. Kujawa & Burkhouse, 2017), consistent with ECI theory.

Present Study

Given the importance of emotion processing in relation to depression-risk, we sought to examine maternal history of depression in relation to emotional face processing in a sample of early adolescent girls. We focused on maternal depression, given research indicating a stronger link between youth functioning and maternal versus paternal depression (Connell & Goodman, 2002), and girls due to gender differences in depression prevalence following early adolescence. We examined emotion processing components reflecting early perceptual processing (N200), and later higher-order processing (N400 and LPP) of happy, sad, and neutral faces that were either forward-facing (e.g. looking directly at the participant), or oriented at a 45-degree angle (e.g. looking away from the participant). For forward-facing stimuli, which have been used in most prior studies of emotion processing in relation to depression-risk, we hypothesized that girls at low-risk for depression (i.e. those with no maternal depression history) would show enhanced

N200, N400, and LPP to happy and sad faces compared to neutral faces, in line with prior 18 research in this area (Bylsma et al., 2008). Conversely, we predicted that girls at high-risk for depression (i.e. those with a maternal depression history) would show undifferentiated

N200, N400 and LPP responses to emotional and neutral faces, as predicted by ECI

(Rottenberg & Hindash 2015). However, we also examined whether maternal depression history would be associated with enhanced N200, N400, and LPP amplitudes specifically for sad (rather than happy) faces, in line with the hypothesis that biased processing of sad faces represents a specific marker of depression risk (Bistricky, et al 2014). Moreover, we hypothesized face-orientation would be more strongly associated with discriminated processing in low-risk compared to high-risk girls. In girls at low-familial risk, we predicted enhanced early and later visual processing responses to positive or negative faces oriented towards versus away from the viewer. However, we predicted that high- risk girls would show diminished responsivity to differences in face-orientation, extending findings related to ECI to differences in personal relevance of emotional stimuli. A competing possibility is that depression risk would be associated with specific enhancements for direct sad faces in high-risk girls, due to enhanced motivational salience, while depression-risk would not be associated with alterations in the less-salient averted sad-faces.

Methods

Participants

EEG data was collected from 63 mother-daughter dyads, although the data from seven dyads was excluded due to recording problems or excessive artifacts (excluded families were not significantly different in demographic variables or depression histories). Final participants were 56 mother-daughter dyads with daughters between the 19 ages of 10 – 14 years (mean daughter age was 12.15 years; SD = 1.33). Mean maternal age was 43.30 years (SD = 5.28). In line with regional demographics, 68% of youth identified as European American, 20% as African American, 7% as Latinx, and 5% as

Asian American. According to maternal report, parents were married or cohabitating in

68.9% of families, and the average household income was between $70,000-$79,999.

Measures

Structured Clinical Interview for DSM-IV TR (SCID-I and K-SADS-PL; First &

Gibbon, 2002; Kaufman et al., 1995). Mothers and daughters completed diagnostic interviews to assess for current or history of Major Depressive Disorder. Mothers were administered the Structured Clinical Interview for DSM IV TR (SCID; First & Gibbon,

2002), and youth were administered the Schedule for Affective Disorders and

Schizophrenia for school-age children-present and lifetime version (K-SADS-PL;

Kaufman et al., 1995). Diagnostic interviews were conducted by trained graduate-level research assistants or licensed clinical psychologist. Only the Major Depressive Disorder sections of the K-SADS and SCID were administered. Interviewers completed didactic training in order to achieve a high level of interrater reliability (kappa > .80), with ongoing meetings to minimize interviewer drift.

Covariates. Mothers completed the 20-item Center for Epidemiological Studies

Depression Scale (CES-D; Radloff, 1977), with high reliability in the current sample (α =

.92). Mothers also completed the 21-item Beck Anxiety Inventory (BAI; Beck & Steer,

1993), with high-reliability observed (alpha = .90), and a demographic form including an item for gross annual household income. Youth completed the Children’s Depression

Inventory (CDI; Kovacs, 2015), a 27-item self-report measure of depressive symptoms, 20 with high-reliability in this sample (α = .91), as well as the well-validated 9-item Pubertal

Development Scale (Peterson, Crockett, Richards, & Boxer, 1988; alpha = .64).

Face Viewing task. Youths participated in a computerized task while EEG data was recorded. A passive-viewing paradigm was employed. This type of face viewing task has been well validated and been used in similar studies, as well (e.g. Foti, Olvet, Klein

& Hajcak, 2010). For the task, subjects were instructed to simply view emotional faces

(Happy, Neutral, and Sad), presented in color on a computer screen. Faces were presented in two orientations, including front-view faces (with the pictured individual looking into the camera), and averted-away (with the face presented at a 45-degree angle from the participant). Subjects were instructed to be “still as a statue” while looking at a cross to orient their view towards the center of the screen where the faces appeared. The task presented 120 images from the Karolinska Directed Emotional Faces set (KDEF;

Lundqvist et al, 1998), in randomized order. Each trial included a 1000ms fixation cross, a 1000ms stimulus presentation, followed by an intertrial interval (mean = 1000ms).

Images were photos of 60 male and 60 female faces, with half of images forward facing and half averted facing (oriented 45° with gaze directed off camera). The task included an equal number of neutral and emotional faces (60 each), with half of the emotional faces presenting happy expressions and half presenting sad expressions.

EEG data acquisition

Continuous EEG data was recorded with a Biopac MP150 system from 11 scalp sites (F3, Fz, F4, C3, Cz, C4, P3, Pz, P4, O1, and O2), a common-ground sensor at FCz, and the right and left earlobes. EEG data was recorded using tin electrodes in an Electro-

Cap International head-cap following the international 10/20 placement system. A left- 21 ear reference was used during recording, and data was re-referenced offline to the average of the right and left ears. Vertical electrooculogram (VEOG) data was recorded with sensors above and below the right eye. Blink artifacts were removed through independent component analyses (ICA; Delorme, Sejnowski, & Makeig, 2007). Electrode impedances were below 5 kΩ. Data was recorded using a sampling rate of 500 Hz and gain of 2000. EEG data was bandpass filtered with cutoffs of .1 – 30 Hz. EEG data was averaged and artifacts were corrected offline using ERP-Lab toolbox (Lopez-Calderon &

Luck, 2014; www.erpinfo.org/erplab) and EEGlab (Delorme & Makeig, 2004; sscn.ucsd.edu/eeglab). Continuous data was epoched for the three affective picture categories across a 200ms baseline and 1000ms picture viewing window.

Procedures

Families were recruited via flyers and online postings in the local community.

Mothers were screened by phone to assess study eligibility (daughter aged 10 – 14 years, mother/legal guardian willing to participate, and fluent English), and mothers completed screening measures for depressive symptoms in themselves and their child, in an effort to over-sample families of mothers with a history of depression but non-depressed youth.

Eligible mother-daughter dyads were invited to participate in a 90-minute lab visit. Prior to the lab visit, participants completed questionnaires assessing demographic information, parenting styles, and history of depression. During the lab visit, trained research assistants conducted separate diagnostic interviews with both parents and their teens regarding their own depression histories. Youths then completed two EEG tasks, only one of which, the Face Viewing task, is presented in the present study. Youths completed this task alone in a temperature controlled, sound-attenuated room, monitored via wall- 22 mounted cameras in an adjacent control room. Families received $50 in compensation for their participation. Consent and assent were obtained from both mother and daughter at the start of the lab-visit. Further, all families were provided a list of referrals and in the case of suicidal ideation a risk assessment was conducted. All procedures were approved by the university IRB.

Analysis Plan

Based on visual inspection and comparison with prior studies amplitude average were calculated during the following time windows post stimulus presentation: N200 amplitude was calculated as the average of 175-250ms, N400 amplitude was calculated as the of 375-450ms, and LPP amplitude was calculated as the average of 550-800ms.

Following preliminary correlational analyses, repeated measures ANOVAs were conducted to examine associations between maternal depression scores and youth ERP amplitude, and included valence (Happy, Sad, Neutral), orientation (straight, averted), and caudality (frontal, central, parietal electrode) as within-subject variables. In line with prior studies that examined these ERP components at frontal to parietal electrode sites, we included three midline electrodes (Fz, Cz, and Pz) (e.g. Auerbach, Stanton, Proudfit,

& Pizzagalli, 2015; Poole & Gable, 2012; Webb, et al 2017). All analyses included maternal depression as a between-subjects variable. All analyses were performed using

SPSS version 25.0; all analyses were considered significant at p <.05 with Greenhouse-

Geiser epsilon corrections, and with Bonferroni-correction on follow-up analyses.

Supplemental analyses examined covariate effects.

Results

Descriptive statistics for depressive symptoms were as follows: CDI (M = 9.0, SD 23

= 7.84); CES-D (M= 10.90, SD = 9.51). Twenty-two mothers met criteria for a current or past diagnosis of depression, 15 of whom self-reported having sought therapy for depression or anxiety in the past. Although mothers completed a brief screening measure

(the parent-report Child Depression Inventory) to screen for depressed youth, four girls met criteria for depression when assessed during the lab visit, three of mothers with depression histories and one without.

Demographic data is presented in Table 1. There were no significant between- group differences on any variables. Figure 1 shows ERPs for averted versus straight trials across emotions for low- and high-risk girls. In a series of bivariate correlations, shown in

Table 2, maternal diagnostic history was significantly relation to maternal depression and anxiety symptoms, but not to any demographic or youth-related variables. Youth depressive symptoms were not significantly related to current maternal depressive symptoms or maternal diagnostic history.

N200 amplitude. Repeated measures ANOVA results for all components are shown in Table 3, means and standard deviations for all components are shown in Table

4. A significant face orientation by maternal depression interaction was observed, F (1,

2 55) = 6.11, p = .017, 휂푝 = .10. In Bonferroni-corrected follow-up analyses, low-risk youths exhibited significantly less negative N200 amplitudes for averted faces (M = -

2.15, SE = .76) than for forward faces (M = -3.72, SE = .83). Conversely, for high-risk youths, the difference between N200 amplitude for averted faces (M = -4.28, SE = .93) versus forward faces (M = -3.74, SE = 1.02) was not statistically significant. No significant differences were found for emotion (see Figure 2).

N400 amplitude. A significant face orientation by maternal depression interaction 24

was observed, F (1, 55) = 4.09, p = .017, ηp2 = .07. In Bonferroni-corrected follow-up analyses, low-risk youths exhibited significantly less negative N400 amplitudes for averted faces (M = -1.68, SE = .81) than for forward faces (M = -3.57, SE = .86).

Conversely, for high-risk youths, the difference between N400 amplitude for averted faces (M = -4.04, SE = .99) versus forward faces (M = -3.99, SE = 1.07) was not statistically significant. No significant differences were found for emotion (see Figure 3).

LPP amplitude. A significant main-effect of maternal depressive history was

2 observed, F (1, 55) = 5.64, p = .021, 휂푝 = 0.09. In Bonferroni adjusted follow-up analysis, low-risk youth exhibited significantly more positive LPP amplitudes (M = .27,

SE = .61), relative to high-risk youth (M = -2.02, SE = .77). This main-effect was qualified by a significant face orientation by maternal depression interaction, F (1, 55) =

2 4.34, p = .042, 휂푝 = 0.07. Bonferroni-corrected follow-up analyses comparing straight and averted faces within risk groups yielded non-significant differences, in contrast to results for the N200 and N400 components. However, Bonferroni-corrected analyses comparing risk groups within straight and averted faces indicated that low-risk youth exhibited significantly more positive LPP amplitudes for averted faces (M = .69, SE =

.59), compared to high-risk youth (M = -2.63, SE = .74). There was no significant difference between risk-groups for forward-oriented faces (high-risk: M = -1.34, SE =

.94; low-risk: M = .17, SE = .74). No significant differences were found for emotion (see

Figure 4).

Supplemental analyses. Additional repeated measures ANOVAs were conducted, including youth depressive symptoms, age, pubertal status, ethnicity, maternal marital status, and maternal anxiety symptoms as covariates. The previously significant effects 25 remained significant for all components. Finally, analyses were re-run excluding four youth with depression diagnoses, and results were unchanged, as all previously reported significant maternal depression by face orientation interactions remained significant.

Discussion

Although depression-risk has been associated with altered responding to emotional faces in youth, there has been little examination of factors that may influence such responding. The current study examined visual processing components in relation to maternal depression history in an early adolescent sample, in response to emotional faces either focused on the participant, suggesting enhanced personal relevance, or away from the participant. In line with ECI theory (Rottenberg & Hindash, 2015), we predicted that high-risk youth would exhibit diminished differential responding to emotional versus neutral faces and to forward-facing versus averted emotional faces. Suggesting decreased sensitivity to contextual information and therefore differences in personal relevance. We also examined the competing possibility that familial depression risk would be associated with enhanced processing specifically of forward-facing sad faces (Bistricky, et al 2014).

Although four youths met criteria for current depression, removing these youth from analyses did not affect the pattern of significant results. Further, correlations indicated no significant relationship between youth and maternal depressive symptoms, and including youth depressive symptoms as a covariate also did not alter the pattern of significant results. Therefore, results were interpreted as reflecting the effects of maternal depression on youth’s attention to affective stimuli.

Results partially supported hypotheses regarding differential responsivity to straight versus averted faces in high-risk (maternal depression history) versus low-risk 26 girls (no maternal depression history). Results regarding the joint effects of maternal depression history and facial orientation were comparable for N200 and N400 amplitudes

(reflecting early structural encoding of faces, and later accessing of knowledge and evaluation of meaning regarding facial emotions, respectively; Bentin et al., 1996;

Olivares et al., 2015). Results for both components were in line with predictions regarding facial orientation effects derived from ECI theory. In particular, we found differentiated N200 and N400 amplitudes to forward versus averted faces, but only in girls of mothers without histories of depression. In these lower-risk girls, faces directed towards the viewer elicited enhanced (i.e. more negative) N200 and N400 amplitudes, compared to N200 and N400 responses to faces directed away from the viewer. These facial-orientation effects in low-risk girls are consistent with the direction observed in prior studies (e.g. Bublatzky et al, 2017; McCarthy, Puce, Belger, & Allison, 1999), and suggest both enhanced early structural encoding (e.g. N200) and later accessing of memory and “meaning” processing (e.g. N400) to the more personally-relevant direct- gaze faces (regardless of emotional category).

By contrast, girls of mothers with a history of depression responded similarly to both direct and averted faces, suggesting they did not selectively attend to faces directed towards versus away from them. Given that maternal depression is associated both with greater interparental conflict and more hostile, critical parenting (e.g. Shelton & Harold,

2008), it may be adaptive for daughters of mothers with histories of depression to be sensitive to emotional faces, whether they are directed towards youth or not. We speculate that such non-discriminated responding may reflect the broad nature of negative emotional conflicts within high-risk family environments, such that heightened 27 attention to emotional cues may be adaptive, regardless of who those emotions are directed towards. Even if such non-discriminated responding in early structural and semantic face processing is adaptive within high-risk family environments, it may ultimately carry longer-term risks, if it ultimately predicts general hypervigilance to emotional faces in extrafamilial situations (e.g. with peers, or at school) where such a pattern may no longer be adaptive. Future research examining this possibility is warranted.

While results suggested non-discriminated responding in early structural and semantic processing stages across direct and averted faces in high-risk girls, results for later higher-order processing, reflected by the LPP, yielded a somewhat different pattern of results. Although there were not significant differences within risk groups regarding responses to straight versus averted faces (as observed for the N200 and N400), high-risk girls did exhibit significantly less positive LPP responses specifically to averted (but not forward-oriented) faces, compared to girls of mothers without a history of depression.

The LPP is suggested to reflect sustained attention and higher-order processing of motivationally important information (Hajcak & Dennis, 2009; Kujawa, et al, 2015). It may be that high-risk girls dedicated greater early processing resources to faces, regardless of personal focus implied by facial orientation/gaze direction (e.g. non- discriminated N200 and N400 amplitudes), in order to identify general signs of threat in the context of more hostile or negative family environments. However, following early non-discriminated responding, they subsequently selectively disengaged from averted faces at elaborative processing stages, as averted faces may be less motivationally salient, suggesting emotions directed at others in the environment. 28

Broadly, the pattern of responding across early and later stages of processing may be interpreted as reflecting a vigilance-avoidance response pattern. We speculate that the non-discriminated early processing of self- and other-directed emotional faces observed in high-risk girls may reflect an adaptive response to family environments often marked by conflict and negativity (Shelton & Harold, 2008). Indeed, a meta-analytic review of the literature noted that maternal depression is associated with increased hostile and coercive behaviors toward their children (Lovejoy, et al 2000). Therefore, hypervigilance for signs of negative emotions may allow adolescent youth to better avoid or cope with these threats. Subsequently, however, high-risk girls disengaged from averted facial stimuli, relative to low-risk girls, suggesting that “other-directed” faces may be screened- out for higher-order processing. Similar patterns of early enhanced processing coupled with later disengagement have been observed in other clinical or at-risk populations.

Indeed, a general pattern of enhanced early processing coupled with later reductions in higher-order processing of emotional stimuli has been observed in individuals with co- occurring depression and alcohol abuse in late adolescence and early adulthood (Connell, et al, 2015), high trait-anxiety (Holmes, Neilson, & Green, 2008), generalized anxiety disorder (Weinberg & Hajcak, 2011), and post-traumatic stress disorder (e.g. Adenauer et al., 2010). Similarly, in a two-year study of anxious youth, aged 9 - 14, sustained avoidance of threat-faces in an emotional dot-probe task predicted greater depressive symptoms over time, highlighting the potential role of emotional-avoidance in relation to depression-risk in early adolescence (Price et al., 2016). It is worth underscoring, though, that our results were related to face orientation, rather than to emotional valence. Our assumption is that face-orientation served as a proxy for motivational relevance, with 29 faces oriented towards the viewer suggesting greater personal relevance than faces oriented away from the viewer, is supported by prior research in healthy populations (e.g.

Bublatzky et al., 2017; Bublatzky & Alpers, 2017).

While results for early and later emotional face processing components were consistent with facial-orientation hypotheses derived from ECI theory, it is worth underscoring that our results were not consistent with emotional valence hypotheses derived from this perspective. Although the emotional face stimuli used in this study has been well-validated, we did not find differences in ERP responses to positive, negative, or neutral facial stimuli for either high- or low-risk youth. Results generally did not support the hypothesis that familial depression risk would be associated with enhanced processing of sad faces (e.g. Bistricky et al., 2014). Indeed, more broadly, we observed few significant differences in N200, N400, or LPP responses to emotional versus neutral faces, in contrast to many studies on emotional face processing. The lack of significant emotion effects may be related to oversampling girls with familial histories of depression

(given that depression-risk is generally associated with non-discriminated responding to emotional versus neutral emotional stimuli; e.g. Bylsma et al., 2008). It is also possible that the lack of discriminated responses to emotional stimuli may be related to the use of a passive-viewing paradigm, which may be associated with diminished task focus, or to the inclusion of averted facial stimuli. Alternatively, to our knowledge, EEG studies of familial depression risk have not focused on facial orientation, and the inclusion of averted and forward faces may affect the typical pattern of emotional responsivity observed in other studies. Further, we employed both male and female faces in the task. It may be that girls respond to male and female faces differently, coloring emotional 30 valence effects (see Kret & Gelder, 2012). Unfortunately, we were unable to examine such effects, as stimulus gender was not recorded during the task.

Limitations and Future Directions

While the current study examines an important area of development in the context of neural processing and depression risk, there are limitations that suggest future avenues for research. First, the current study relies on cross-sectional data, and longitudinal work in this area is needed. Second, we examined 10-14-year-old female youth, which covers significant pubertal development. Although controlling for pubertal status did not alter the results, more targeted examination of pubertal effects may be warranted. Third, we did not include fathers or sons in the study, and future examination of depression-risk in males would extend our understanding of youth emotional processing in relation to parental depression. Further, although dyads were screened for maternal reports of low youth depressive symptoms, four girls met criteria for depression during more intensive lab-based interviews. Removing these youths from analyses did not affect the pattern of results, however, but future work examining the impact of youth depression on facial orientation effects is needed. Finally, we examined a relatively limited range of emotional stimuli (happy, sad, and neutral). Although this narrow range was useful in terms of minimizing task length, future work should examine a broader range of affective stimuli

(e.g. anger, fear) to examine potential differences in face direction across a wider range of emotional stimuli.

Despite limitations, our findings add new information to the literature on emotional processing in relation to depression-risk, highlighting the potential role of face direction in altered responding to emotions. Youth at-risk for depression were less-likely 31 to exhibit discriminated responding to self- versus other-directed emotions at early processing stages, suggesting early attentional vigilance to emotions (regardless of direction), but later decrements in processing specifically for averted-faces, suggesting specific pattern of disengaging from other-directed emotions at later-stages of processing.

We have speculated that the non-discriminated early N200 and N400 results for high-risk youth may suggest the adaptive importance of broad attention towards emotions, regardless of target, given that maternal depression has been associated with a broad pattern of heightened interparental and parent-child conflict and hostility. Future research examining this possibility more directly is warranted. 32

Appendix

Face viewing task

Neutral Forward

1000ms

+ ITT + Fixation Cross + 1000ms Sad Forward Neutral Averted 1000ms 1000ms

ITT + Fixation Cross + + ITT + Fixation Cross 1000ms 1000ms Sad Averted

1000ms 1000ms + ITT + Fixation Cross

1000ms

Center for Epidemiological Studies – Depression Scale

rev. 12/7/05 CESDD (57) Adolescent Depression Family Treatment Study Page 1 of 1

Family: A D Resp: Father Mother 2nd Male Parent 2nd Female Parent

Date: / / 2 0 0 Int #: Mark choices like this: Wave: 1 2 3

INSTRUCTIONS: Fill in the circle for each statement that best describes how often you felt this way during the past week.

Some or a Occasionally Rarely or none little of or a moderate Most or all of the time the time amount of time of the time During the past week. . . (0-1 day) (1-2 days) (3-4 days) (5-7 days) 1. I was bothered by things that usually don't bother me. 2. I did not feel like eating; my appetite was poor. 3. I felt that I could not shake off the blues, even with help from my family or friends. 4. I felt that I was just as good as other people. 5. I had trouble keeping my mind on what I was doing. 6. I felt depressed. 7. I felt that everything I did was an effort. 8. I felt hopeful about the future. 9. I thought my life had been a failure. 10. I felt fearful. 11. My sleep was restless. 12. I was happy. 13. I talked less than usual. 14. I felt lonely. 15. People were unfriendly. 16. I enjoyed life. 17. I had crying spells. 18. I felt sad. 19. I felt that people disliked me. 20. I could not "get going."

186

Child Depression Inventory (CDI)

Table 1. Means for demographic and diagnostic characteristics of the youths and their parents. Includes means for all participants, as well as high risk group (maternal depression history) and low risk (no maternal depression history).

Total (N=56) High Risk (N=22) Low Risk (N=34) Parent Age 43.30 (5.28) 40.78 (8.19) 43.29 (5.26) Average income 70-79,999$ 60-69,999$ 70-79,999$ Married/Cohabitating 68.9% 65.2% 72.9% Maternal Depressive 11.05 (9.62) 15.43 (11.60) 7.94 (6.78) Symptoms (CESD) Maternal Anxiety 7.57 (7.04) 11.65 (8.64) 4.89 (4.01) Symptoms (BAI)

Youth Age 12.55 (1.33) 11.87 (1.32) 11.62 (1.31) European-American 68% 73% 63% African-American 20% 23% 22% Latinx 7% 4% 5% Asian-American 5% 0% 10% Youth Depressive 9.05 (7.90) 10.09 (9.02) 8.37 (7.13) Symptoms (CDI)

.20

.23

correlations, between and

.15 --

.29* .26* .02

- -- - -

biserial

.03

.17 .12 - .03

.25 .10

.14 8. -- .61* - -

-- .10 7. -- .12 .01 .06 .09

.07 .01 .11 .01

- 6. -- - .17 - .43* -

.01 .01 .03 .23

- 5. .34* - - - .57* .15

.12 .16

- 4. -- - .07

coefficients. coefficients.

. Bivariate correlations Bivariate .

.02

3. -

Table Table

tailed).

Family income Family residualized) status (age pubertal Youth 1. CES Maternal diagnostic history Maternal symptoms depressive Youth status minority Ethnic cohabiting / married Mother symptoms anxiety Maternal age Youth

4. 8. 1. 2. 3. 5. 6. 7. 9. Correlations Note: between categorical continuous and are variables point categoricalvariables phi are * p 0.05 < (2 39

Table 3. Repeated measures ANOVA with maternal depression history as a between subjects variable. Note: Statistically-significant effects are bolded.

Table 4. Descriptive Statistics for N200, N400, & LPP Amplitudes.

N200 N400 LPP Mean SD Mean SD Mean SD Straight Happy Fz -5.94 6.49 -6.86 6.70 -3.42 6.71 Cz -4.80 6.49 -4.73 6.54 -.56 6.49 Pz -.30 7.35 1.77 7.73 3.81 6.90

Calm

Fz -5.94 6.19 -6.96 6.19 -4.07 7.39

Cz -4.67 6.54 -5.03 6.43 -.68 7.09 Pz .76 6.89 2.06 6.65 4.14 8.00 Sad Fz -6.55 8.24 -7.10 5.72 -3.43 5.46 Cz -5.33 7.83 -3.47 6.37 -1.22 5.43 Pz -.52 7.79 5.19 7.00 2.85 5.66

Averted Happy Fz -6.36 5.70 -7.65 6.22 -4.62 5.14 Cz -4.22 6.16 -4.36 6.48 -1.13 5.33 Pz 2.12 8.30 4.72 7.74 3.90 4.92

Calm

Fz -6.06 5.84 -8.11 7.99 -4.74 7.27 Cz -3.95 6.18 -5.78 7.74 -.59 8.78 Pz 2.14 6.51 .93 8.35 4.35 9.77 Sad Fz -7.18 7.16 -7.81 7.86 -4.79 6.46 Cz -4.98 6.47 -5.35 6.82 -1.29 6.50 Pz 1.88 7.06 4.12 7.24 4.54 7.22 41

risk girls girls risk

- appy

d ERPs for straight and averted faces across across d and faces averted ERPsstraight for

ad girls are shown and black, in are high for girls

risk risk - verage

re 1. Grand 1. re a Grand

emotions and risk and groups. emotions

Figu

Note: ERPs low for Note: dashed and lines averted denote lines faces, forward denote Solid red. in faces. Neutral 42

Figure 2. N200 amplitude for averted vs. forward oriented faces in high risk (maternal depression history) and low risk (no maternal depression history) youth averaged across electrodes Fz, Cz, and Pz. Error bars reflect the standard error of the mean.

0 Forward Faces Averted Faces -1

-2

-3 High Risk Low Risk -4

Average N200 (uV) N200 Average Amplitude -5

-6 Face Orientation

Figure 3. N400 amplitude for averted vs. forward oriented faces in high risk (maternal depression history) and low risk (no maternal depression history) youth averaged across electrodes Fz, Cz, and Pz. Error bars reflect the standard error of the mean.

0 Forward Faces Averted Faces -1

-2

-3 High Risk Low Risk -4

Average N400 (uV) N400 Average Amplitude -5

-6 Face Orientation

1.5 1 0.5 0 Forward Faces Averted Faces -0.5 -1 High Risk -1.5 Low Risk -2

Average LPP Amplitude LPP (uV) Average Amplitude -2.5 -3 -3.5 Face Orientation

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