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Quevedo 2016
Quevedo 2016
CITATION
Quevedo, K., Ng, R., Scott, H., Martin, J., Smyda, G., Keener, M., & Oppenheimer, C. W. (2016,
September 12). The Neurobiology of Self-Face Recognition in Depressed Adolescents With Low
or High Suicidality. Journal of Abnormal Psychology. Advance online publication. http://
dx.doi.org/10.1037/abn0000200
Journal of Abnormal Psychology © 2016 American Psychological Association
2016, Vol. 124, No. 4, 000 0021-843X/16/$12.00 http://dx.doi.org/10.1037/abn0000200
This study sought to test whether the neurobiology of self-processing differentiated depressed adoles-
cents with high suicidality (HS) from those with low suicidality (LS) and healthy controls (HC; N ⫽ 119,
MAGE ⫽ 14.79, SD ⫽ 1.64, Min ⫽ 11.3, Max ⫽ 17.8). Participants completed a visual self-recognition
task in the scanner during which they identified their own or an unfamiliar adolescent face across 3
emotional expressions (happy, neutral or sad). A 3-group (HS, LS, HC) by 2 within-subject factors (2 Self
conditions [self, other] and 3 Emotions [happy, neutral, sad]) GLM yielded (a) a main effect of Self
condition with all participants showing higher activity in the right occipital, precuneus and fusiform
during the self- versus other-face conditions; (b) a main effect of Group where all depressed youth
showed higher dorsolateral prefrontal cortex activity than HC across all conditions, and with HS showing
higher cuneus and occipital activity versus both LS and HC; and (c) a Group by Self by Emotion
interaction with HS showing lower activity in both mid parietal, limbic, and prefrontal areas in the Happy
self versus other-face condition relative to the LS group, who in turn had less activity compared to HC
youth. Covarying for depression severity replicated all results except the third finding; In this subsequent
analysis, a Group by Self interaction showed that although HC had similar midline cortical structure
(MCS) activity for all faces, LS showed higher MCS activity for the self versus other faces, whereas HS
showed the opposite pattern. Results suggest that the neurophysiology of emotionally charged self-
referential information can distinguish depressed, suicidal youth versus nonsuicidal depressed and
healthy adolescents. Neurophysiological differences and implications for the prediction of suicidality in
youth are discussed.
Keywords: suicidality, brain function, self-processing, self-face, adolescence, midline cortical structures
Suicide is the second leading cause of death in the United States ranging from ideation to nonlethal self-injuries with the intent to
among youth aged 10 –24 years (Murphy, Xu, & Kochanek, 2010). die, to actual attempts and completions (Brezo, Paris, & Turecki,
The adolescent transition in particular is associated with a dramatic 2006; Nock et al., 2013). Although suicide is a preventable cause
increase in suicidality, defined as all suicide related behavior of death, efforts to reduce its occurrence have had little success
1
2 QUEVEDO ET AL.
(Singh & Yu, 1996), in part because of limited ability to accurately show preferential endorsement of negative self-referential infor-
predict suicide risk. Major depressive disorder is one of the most mation, and avoidance or neglect of positive self-referential ma-
well established risk factors for suicidality among youth. Clinically terial.
depressed youth are six times more likely to attempt suicide than
nondepressed youth (Nock et al., 2013). Given the high rates of
Relevance of Self-Face Processing for Understanding
suicide attempts and completions among depressed adolescents,
Suicide Risk
identifying predictors of suicidality within this clinical population
is essential. Assessment of suicide risk currently relies almost Self-face processing is a discrete modality of self-referential
exclusively on self-report interviews and questionnaires, ap- processing, and humans show a distinct response to their own face
proaches that are limited by the fact that many individuals are poor compared to those of other familiar and stranger faces, as con-
reporters of their own suicidal behavior (Nock et al., 2010), and firmed by preferential processing of self-faces during face recog-
many who report suicidal thoughts never attempt suicide (Pokorny, nition paradigms (Ma & Han, 2010). Critically, in healthy adults,
1983). Clinical neuroscience can begin to address these limitations self-face recognition activates implicit rewarding and positive self-
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
to suicide diagnosis and prevention by uncovering more objective perceptions typical of normative self-processing (Blackwood et al.,
This document is copyrighted by the American Psychological Association or one of its allied publishers.
biomarkers of suicide risk. Identifying key neural circuits distin- 2003; Drake & Seligman, 1989). These positive self-biases facil-
guishing depressed youth with high suicidal ideation from other itate more rapid behavioral responses to the self-face (Ma & Han,
depressed youth and psychologically healthy controls may help to 2010). Thus, normative self-face recognition is biased toward
better predict suicide risk. Research further suggests that disturbed positively valenced information and faster preferential responses
self-referential processing may contribute to increased risk for to the self-face over the faces of others.
suicide (Burke et al., 2016). However, it remains unknown how However, evidence supports that one’s self-schema influences
neural alterations during self-referential processing are associated the processing of the self-face. For example, low levels of positive
with suicidality. Thus, the main purpose of this study was to self-appraisals contribute to less preferential bias for one’s own
examine neural function during processing of emotional self-faces face (Ma & Han, 2010) and a negative attributional style is linked
(vs. faces of others) among depressed, suicidal adolescents. to faster RTs to one’s own sad facial expression (Caudek & Monni,
2013). Given that biased self-schemas and self-referential process-
ing biases are prevalent among depressed and suicidal youth,
Self-Referential Processing Biases and Suicide Risk
atypical processing of self-faces may be characteristic of youth at
Cognitive theories emphasize the role of self-schemas in vul- risk for suicide. Prior research has established that attention, per-
nerability for suicide (Alloy, Abramson, Safford, & Gibb, 2006; ception, and identification biases for affective facial stimuli are
Beck, 1961), positing that negative self-schemas increase suicide robust among youth with emotional disorders and symptoms,
risk by influencing the perception, encoding, retrieval, and inter- including suicidality (Hankin et al., 2010; Joormann, Gilbert, &
pretation of self-referential cues (Burke et al., 2016; Wenzel & Gotlib, 2010; Seymour et al., 2016), although these studies have
Beck, 2008). Evidence also suggests that individuals at risk for not focused on self-faces specifically. Emotional facial stimuli are
suicide are more likely to have negatively biased self-cognitions. frequently used in these information processing studies, because
For example, suicidal individuals, including adolescents, are more processing of facial emotional expressions are rapid and automatic
likely to have negative self-appraisals and to make more self- (Vuilleumier & Schwartz, 2001), and are believed to function
attributions about the causes of negative events compared to non- external to awareness (Gotlib & Neubauer, 2000). Taken together,
suicidal controls (Brunstein Klomek et al., 2007; Tang, Wu, & research suggests that identifying one’s own emotional self-face
Miao, 2013). Furthermore, depressed individuals, who are typi- may be a useful and rigorous approach for assessing potential
cally at higher risk for suicide than psychologically healthy con- abnormal neurophysiology during emotional self-referential infor-
trols, show preferential processing of negative self-referential ma- mation processing among suicidal youth.
terial such as greater recall of negative self-referential trait
adjectives, faster RTs to negative self-referential stimuli, and pref-
Neurobiology of Self-Face Processing and Suicide Risk
erential attention to negative emotional stimuli, including facial
emotional expressions (Fritzsche et al., 2010; Greenberg & Alloy, The neurobiology of self-referential and emotional face process-
1989). ing can inform hypotheses about which alterations in neural cir-
Depressed or depression-prone individuals are also significantly cuitry during processing of emotional self-faces versus other-faces
less likely to endorse and correctly recall self-referential positive may be associated with suicide risk. Neural core components of
information, and exhibit greater attentional avoidance to positive face perception include the occipital inferior gyrus, lateral fusiform
facial expressions than psychologically healthy individuals (Alloy, gyrus, and superior temporal sulcus (Stuhrmann, Suslow, & Dann-
Abramson, Murray, Whitehouse, & Hogan, 1997; Gotlib, Kras- lowski, 2011). Brain regions typically involved in the experience
noperova, Yue, & Joormann, 2004; Hankin, Gibb, Abela, & Flory, and production of emotions are also implicated in the processing of
2010). A recent study of adolescents showed that youth with facial information (Stuhrmann et al., 2011), including limbic areas
suicidal ideation were also more likely to endorse negative self- such as the amygdala, hippocampus, insula, and thalamus (Kircher
traits and less likely to endorse positive self-traits compared to et al., 2001; Sugiura et al., 2008; Uddin, Kaplan, Molnar-Szakacs,
adolescents without suicidal ideation during a self-referential pro- Zaidel, & Iacoboni, 2005). Finally, and of particular importance,
cessing task, even after controlling for clinical depression (Burke midline cortical structures (MCS) such as the medial prefrontal
et al., 2016). Overall the extant research suggests that, in contrast cortex (MPFC) including BA 9 and 10, anterior cingular cortex
to psychologically healthy individuals, those at risk for suicide (ACC), and posterior cingulate cortex (PCC) are involved in
NEUROBIOLOGY SELF-FACE SUICIDAL YOUTH 3
self-face processing and the processing of self-referential or auto- In sum, although a number of studies demonstrate atypical
biographical information (Hu et al., 2016; Murray, Debbane, Fox, self-referential processing in depressed youth, researchers have
Bzdok, & Eickhoff, 2015; e.g., self-traits, own name, own voice, typically not assessed corresponding associations with suicidality
etc.). Thus, these structures are identified as key areas in the neural in these individuals. However, there is emerging research showing
bases of self-processing that are also involved in the processing of that suicidal individuals have highly biased self-schemas, are more
the self-face versus other-faces (Araujo, Kaplan, & Damasio, likely to endorse negative self-attributions, and more negative than
2013; Fossati et al., 2003). There is also strong evidence that positive self-traits, even above and beyond the impact of depres-
self-face processing involves increased activity localization in the sion (Brunstein Klomek, et al., 2007; Burke et al., 2016; Tang et
right hemisphere of MCS (Sugiura, 2015). al., 2013). Additionally, there is evidence that youth suicide at-
Less is known about neural alterations in response to self-faces tempters, relative to depressed nonsuicidal youth, exhibit aberrant
among individuals with emotional disorders who are at high risk neural responses to emotional faces in MCS and limbic structures
for suicide. Individuals with major depression appear to typically (for example, ACC; Pan et al., 2013), which are thought to play a
exhibit hyperactivity in MCS at rest and during neural tasks key role in the processing of self-information and emotionally
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
compared to psychologically healthy controls, possibly because of valenced stimuli. Therefore, evidence suggests that depressed,
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persistent high levels of negative, self-focused rumination that suicidal youth (e.g., youth who endorse intense suicidal thoughts
characterizes both depression and suicide risk (Nejad, Fossati, & or recent suicide attempts) may demonstrate more intense biases to
Lemogne, 2013). Research further suggests that depressed indi- self-referential information, especially to emotionally valenced
viduals may exhibit heightened activity in MCS, and in emotion- self-information, compared to depressed youth with low levels of
related brain areas during self-referential processing in particular suicidality, Yet, it remains unknown how neural function during
(Grimm et al., 2008; Lemogne et al., 2009; Renner et al., 2015). processing of self-faces is associated with suicidality among youth.
However, although some studies have found hyperactivity in these
areas in depressed patients (Lemogne et al., 2009; Wagner, The Current Study
Schachtzabel, Peikert, & Bär, 2015), others have found hypoac-
tivity (Grimm et al., 2008; Hooley et al., 2009; Johnson, Nolen- This study is the first to examine the neural substrates of
self-referential processing of suicidal individuals. We employed a
Hoeksema, Mitchell, & Levin, 2009; Renner et al., 2015). Overall,
novel task, based on prior work by Kircher et al. (2001), to assess
reviews of the scientific literature suggest the possibility of hyper-
neural processing of positive and negative self-referential stimuli
active MCS during self-referential processing in depression (Nejad
among clinically referred and healthy adolescents. Specifically,
et al., 2013), but mixed findings may be at least partly due to the
depressed adolescents with high and low levels of suicidality, and
limitations of some studies in which the valence of self-referential
psychologically healthy controls, viewed images of the self-face
information was not accounted for in the research design.
versus the face of an unfamiliar adolescent across three different
In studies examining neural responses to valenced emotional
emotional conditions: happy, sad, and neutral. We used images of
faces, a more reliable pattern of activity is associated with higher
self- and other- emotional faces, given that emotional face pro-
risk for suicide. Specifically, depressed individuals exhibit hyper-
cessing tasks have proven to be valid and reliable approaches to
activation to mood-congruent or negative expressions in unfamil-
assess processing biases and atypical neural functioning among
iar faces, but hypoactivity to positive facial expressions, particu- individuals with depression and suicidality (Pan et al., 2013;
larly in the amygdala, insula, parahippocampal gyrus, fusiform, Stuhrmann et al., 2011).
and putamen, as well as the orbitofrontal cortex (Stuhrmann et al., This research was guided by five hypotheses. First, we expected
2011). Similarly, Yoshimura and colleagues (2014) showed that higher right sided MCS activity to self- versus other- faces regard-
depressed patients exhibited a heightened response to negative less of diagnostic group, in addition to greater activity in limbic
self-referential traits in the MPFC and ventral anterior cingulate and other core areas of face processing. Second, we predicted a
cortex, compared to healthy controls, but blunted activation in main effect of diagnostic group whereby depressed youth (both
these areas to positive self-traits. This suggests that among de- high and low suicidality) would show higher activity in MCS than
pressed populations, biases to more self-relevant emotional expres- healthy controls across all conditions (Nejad et al., 2013). Third,
sions (i.e., negative emotions) may involve greater limbic and we expected that brain activity in both MCS and limbic structures
MCS activity, but blunted activity in these regions to less self- during the recognition of the happy self-face versus identification
relevant emotions (e.g., happy faces). In one of only three studies of another youth’s happy face would differentiate depressed youth
examining the neural correlates of suicidality among adolescents, with high versus low suicidality and healthy controls. Specifically,
Pan and colleagues (2013) found that depressed adolescent suicide we hypothesized that highly suicidal depressed youth would dem-
attempters showed greater neural activation to negative expres- onstrate lower activity during happy self-face recognition versus
sions in the faces of others (i.e., angry faces) compared to de- identification of other happy faces. Fourth, we predicted that
pressed nonattempters or healthy controls, but less activation to highly suicidal youth would show greater MCS and limbic activity
happy faces in emotion-related brain areas (e.g., ACC, primary during recognition of the sad self-face versus identification of
sensory cortex, thalamus). These findings support a possible hy- another youth’s sad face. Fifth, we expected that the neurobiology
peractivity to negative emotional expressions in structures in- of emotional self- versus other- face processing would be affected
volved in emotional face processing, and blunted activity to pos- by high suicidality (as previously hypothesized) even after con-
itive facial expressions among depressed and suicidal youth. trolling for effects of self-report measures of explicit self-
However, neural reactivity to self-faces specifically has not been representation (e.g., attributional style) and for clinical variables
specifically examined in this regard. such as medication and depression severity.
4 QUEVEDO ET AL.
Table 1
Demographics and Clinical Variables: Depressed With Low or High Suicidality and Healthy Control Groups
Puberty: M (SD) 2.90 (.62)a 3.04 (.61)ab 3.20 (.41)b F(2, 118) ⫽ 3.16ⴱ
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Faces were displayed for 2 s followed by a 0.5 s fixation cross. alter the HRF for the predominant block self condition. Stimuli,
Each block contained faces of primarily just high or just low accuracy of recognition, and reaction time (RT) data were respec-
degrees of morphing between the self and the other face. This tively presented and concomitantly recorded with E-prime soft-
resulted in blocks comprising self faces or unfamiliar faces within ware (Schneider, Eschman, & Zuccolotto, 2012).
happy, sad, or neutral expression groupings, with the following Neuroimaging data acquisition. Neuroimaging data were
means and standard deviation of morphs: Self blocks: Mself ⫽ 83%, collected using 3.0 Tesla Siemens Trio MRI scanners in Mpls and
SD ⫽ 12%, Minself ⫽ 65%, Maxself ⫽ 100%; Other blocks: Pgh. Structural 3D axial MPRAGE images were acquired in the
Mself ⫽ 18%, SD ⫽ 12%, Minself ⫽ 0%, Maxself ⫽ 35%. Blocks same session (TR/TE: 2,100 ms/3.31 ms; TI: 1,050; Flip Angle 8°;
were presented in five counterbalanced task orders, and each FOV: 256 ⫻ 200 mm; Slice-Thickness: 1 mm; Matrix: 256 ⫻ 200;
contained 28 photos of faces presented randomly with regards to 176 continuous slices). Mean blood oxygenated level depended
morphing percentages within any given self by emotion block. activity (BOLD) images were acquired with a gradient echo EPI
More ambiguous stimuli (i.e., with 40%– 60% of self-features) sequence t ⫽ 16:05 min covering 60 oblique axial slices (2 mm;
were not used in any block. Within each of the six blocks, four TR/TE ⫽ 3,340/30 ms; FOV ⫽ 200 ⫻ 200 mm; matrix ⫽ 80 ⫻
faces were shown of high opposite percentage to the predominant 80; Flip Angle ⫽ 90°).
block self condition to avoid response sets and keep the partici- Participants included had imaging data with xyz axis ⬍2 mm (3
pants engaged (Other block four faces ⫽ 90% or 80% self; Self translation absolute values) and pitch, roll, and yaw rota-
block four faces ⫽ 90% or 80% other) using methods adapted tions ⬍0.587 radians (3 rotation absolute values) shifts. The cur-
from Kircher et al. (2001). The hemodynamic response function rent sample (N ⫽ 119) did not include 5 participants who violated
(HRF), upon which neuroimaging is based on, lasts about 12 s and the movement parameters. Movement parameters for averaged
peaks after approximately 5– 8 s (Kruggel & von Cramon, 1999). translation and rotation parameters did not differ between the two
Thus, brief exposure (2 s) to these “opposite” faces is too fast to sites (Mpls vs. Pgh), F(1, 118) ⫽ 0.31, p ⫽ .60, or between study
6 QUEVEDO ET AL.
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Figure 1. Emotional Self Other Morph-Query (ESOM-Q) Task. Participants indicated if the face looked like
them or not via button press in response to faces with high or low percentage of self features presented randomly
within six blocks across three different expressions (happy, sad, neutral). Minimum self in high self blocks is
65%, and maximum self in high other face blocks is 18%.
groups, F(2, 118) ⫽ 1.4, p ⫽ .25. However, ART software was during recognition of the self or other face conditions across three
used to detect volumes that were outliers (movement ⬎2 mm and emotions. This second level random-effects repeated measure
rotations ⬍0.587) or that had global signal intensities greater than ANOVA with between- and within-group factors, as well as sub-
9 (Mtrials sensored ⫽ 4.08, SD ⫽ 3.2). These volumes were then ject level effects, included the following: a between-group factor,
regressed out of analyses in 1st level GLM analyses described Group (HS, LS, HC) and 2 within-subjects factors, Self (Self,
below. The 3 groups were compared in mean numbers of volumes Other) and Emotions (happy, neutral, sad). This GLM analysis
present with high movement and were not statistically different, allowed us to test main effects of group and conditions, and
F(2, 117) ⫽ 2.12, p ⫽ .12. Frequency of participants with any group by conditions interactions. To test the direction and
number of volumes with unacceptable parameters were compared meaning of significant interaction effects, follow-up contrasts
between groups and did not differ, 2(2, 118) ⫽ 1.36 p ⫽ .51. compared HS to LS to HC for activity during the self condition
Additionally, temporal signal to noise ratios were calculated using for the separate emotions. For example, a Group (HS, LS, HC)
the 3dTstats in Afni by dividing the mean baseline estimate (sig- by Self condition (Self, Other) for just the happy emotional
nal) by the standard deviation of the residual time series (noise) for expression would clarify a previous Group by Self interaction.
the task. These values were extracted analyzed with a t test In SPM8, similar ANOVAs with Group (HS, LS, HC), Self
comparing the sites (Pgh vs. Mpls), which yielded no significant condition (Self, Other), and Emotions (happy, sad, neutral) as
differences, t(596) ⫽ 2.13, p ⫽ .98. between- and within-subjects factors were conducted with and
without depression severity as a covariate (clinician report:
Data Analysis CDRS, or self-report: MFQ), and results are reported accord-
Neuroimaging data processing. Data were preprocessed and ingly. Results for severity measured by clinician or by self-
analyzed with Statistical Parametric Mapping software, Version-8 report yielded similar brain activity differences.
(SPM8; http://www.fil.ion.ucl.ac.uk/spm). Data for each partici- Only whole brain level analyses were conducted, and region
pant were realigned to the first volume in the time series to correct labeling was confirmed by both the xj-view GUI in SPM8 and
for head motion. Realigned images were coregistered with the Talairach Daemon software. To correct for multiple compari-
subject’s anatomical image, segmented, normalized to standard sons, we calculated whole-brain, voxel-wise, and cluster extent
Montreal Neurological Institute template, and spatially smoothed thresholds via Monte Carlo simulations using 3dClustSim in
with a Gaussian kernel of 7 mm full-width at half-maximum. AFNI and an inherent smoothness of 12.23 15.25 13.93 esti-
Trials were modeled with the Canonical Hemodynamic Response mated via the AFNI 3dFWHMx function. This resulted in a
Function. voxel-wise threshold of p ⬍ .001 and the following cluster-
Neuroimaging data analyses. First-level fixed-effect models extent threshold corresponding to p ⬍ .01, FWE-corrected: k ⬎
(GLMs) for each subject and condition at each voxel were calcu- 120.7 voxels for analyses without depression severity as a
lated using a t-statistic producing statistical images for six basic covariate and 130.2 voxels for analyses with depression sever-
contrasts: self-face (happy-baseline, neutral-baseline, and sad- ity included as a covariate. Only group, condition, and group by
baseline) and other face (happy-baseline, neutral-baseline, and condition interaction effects with clusters exceeding those
sad-baseline). Volumes with high movement parameters were re- thresholds are reported. Because almost all HS were recruited in
moved during the first level GLMs using ART software. Groups Mpls, analyses were repeated only for participants from Mpls
were then compared via a second level flexible full factorial GLM (HC ⫽ 21, LS ⫽ 23, HS ⫽ 40) in SPM8. Notably, similar
on the t-contrast images generated by first-level subject level results to the ones reported with the entire sample (both Pgh and
analyses to examine BOLD signal differences between groups Mpls participants) were obtained: Effects of Group: F(2,
NEUROBIOLOGY SELF-FACE SUICIDAL YOUTH 7
486) ⫽ 21.291, p ⬍ .001; Self Condition: F(1, 486) ⫽ 29.23– 696) ⫽ 32.53–24.40, p ⫽ .001– 0.42, and in the thalamus, F(1,
27.89, p ⬍ .001; and Group ⫻ Self and Group ⫻ Self ⫻ 696) ⫽ 24.40, p ⬍ .001 (see Table 2, Figure 2). Follow-up t test
Emotion Interaction: F(4, 486) ⫽ 20.23–20.89, p ⬍ .001. Given contrasts demonstrated that all participants exhibited higher activ-
that signal-to-noise ratios were similar between sites and that ity in these areas for the self face more than for the other face,
key findings were similar for just the Mpls site, results are t(1,696) ⫽ 6.75, p ⬍ .001. All effects remained significant when
reported with the whole sample across both scanning sites. severity of depressive symptoms was covaried in the SPM8 anal-
Covariate and medication effects. Time series for the first yses. Furthermore, no other covariates (attributional style, IQ, or
eigenvalues centered in 7 mm spheres for coordinates of significant scanning site) were significantly associated with neural activity in
differences were extracted for use in graphs and to test if differences those regions, F(1, 109) ⫽ 0.00 – 0.3, p ⫽ .11– 0.85, and the main
remained after controlling for covariates that differed between the effect of the self remained significant when covariates were in-
depressed participants, as well as to examine the role of gender and clude in the model, F(1, 105) ⫽ 22.77, p ⬍ .01. An effect of
task order using SPSS software (IBM SPSS Statistics for Windows, gender showed that females had more brain activity in these areas
Version 22.0). Variables that differed between groups (scanning site, than males, F(1, 105) ⫽ 5.23, p ⬍ .05, yet principal findings held
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IQ, attributional style) were used as covariates in these follow-up when controlling for gender. There were no effects due to task
This document is copyrighted by the American Psychological Association or one of its allied publishers.
analyses, which were similar to those conducted within SPM8, 3 order, F(3, 105) ⫽ 0.24, p ⫽ .87.
Group (HS, LS, HC) by within-subject factors, 2 Self condition (Self, Main effect of group. The omnibus test yielded main effects
Other) by 3 Emotions (happy, neutral, sad) for the varied brain areas of group across all self and emotion conditions in a large cluster
of significant activity differences between groups yielded by SPM8 that encompassed the bilateral cuneus and middle occipital gyrus,
full factorial analyses. Medicated versus unmedicated depressed
F(2, 696) ⫽ 23.34, p ⬍ .001, and in the right frontal inferior gyrus
youth were also compared in brain activity using SPSS software,
(BA9), F(2, 696) ⫽ 14.41, p ⬍ .001 (see Table 2, Figure 3).
which unlike SPM 8, allows to test the significance of covariates in
Follow up t tests contrasts clarified that this was due to HS youth
GLM models.
showing higher activity in the bilateral cuneus and middle occipital
Behavioral response analyses. Analyses were conducted to
gyrus cluster versus LS depressed and HC youth, who did not
test whether observed differences in brain activity were accounted for
differ from one another in activity in these occipital areas,
by behavioral differences. Reaction time (RT) and accuracy of self-
t(1,696) ⫽ 6.75, p ⬍ .001. Follow-up t tests also demonstrated that
recognition (0 ⫽ wrong, 1 ⫽ right) were examined, and the cut-off for
both depressed groups, HS and LS, showed higher activity versus
accurate self-face recognition was correct identification for faces that
had 65% or more of self features. RT and accuracy were examined with HC in the right frontal inferior gyrus (BA9) tha corresponded to
SPSS software and tested with mixed repeated-measures ANOVAs: the right dorsolateral prefrontal (DLPFC) area, t(1,696) ⫽ 5.36,
Group (HS, LS, HC) by Self (self, other) by Emotions (happy, neutral, p ⬍ .01. The reported main effect of group in occipital areas and
sad), similar to the analyses conducted for brain function in SPM8. DLPFC activity was also significant when severity of depressive
symptoms (measured via either the CDRS or the MFQ) was
entered as a covariate in SPM8.
Results
When other covariates were examined, IQ was not significantly
associated with neural activity in the regions specified above, F(1,
Neuroimaging Results
104) ⫽ 2.61–1.14, p ⫽ .109 – 0.853. However, attributional style
Main effect of self condition. Main effects of self condition was a significant covariate, F(1, 104) ⫽ 4.26, p ⬍ .05, with higher
were found in the right occipital, precuneus, and fusiform, F(1, values predicting lower cuneus activity left and right, r ⫽ ⫺0.21
Table 2
Neural Areas That Distinguish High Suicidality vs. Low Suicidality Depressed vs. Healthy Control Youth During Self and Other
MNI
Group Main Effect Cluster Size (K) p(K) Hemisphere x y z F p
Cuneus, Middle Occipital Gyrus HS ⬎ LS ⫹ C 3,544 .000 Left and Right ⫺10 ⫺98 16 23.34 .000
Inferior Frontal Gyrus, BA9 HS ⫹ LS ⬎ C 121 .000 Right 50 18 26 14.41 .036
MNI
Self Condition Main Effect Cluster Size (K) p(K) Hemisphere x y z F p
MNI
Group by Self vs. Other Condition by Happy
Facial Expression Interaction Contrast Cluster Size (K) p(K) Hemisphere x y z
Figure 2. The self face condition is associated with higher posterior midline cortical structures and thalamus
activity versus the other face condition across all emotions and groups. See the online article for the color version
of this figure.
and ⫺0.34, ps⬍0.05. The effect of scanning site was also signif- SPM8, the group by self by emotion interaction was no longer
icant (Pgh vs. Mpls), F(1, 104) ⫽ 8.26, p ⬍ .01, with higher left significant.
and right cuneus activity linked to Mpls participants, r ⫽ .4 and For the brain areas that characterized the group by self by happy
0.5, ps ⬍0.01, respectively. However, the reported main effect of emotion interaction, none of the covariates (IQ, site, or attribu-
Group on cuneus and DLPFC also remained significant, F(2, tional style) were significantly associated with the regions speci-
104) ⫽ 3.65, p ⬍ .05. There were no main effects or interactions fied above, F(1, 110) ⫽ 0.08 –2.79, p ⫽ .11– 0.10, but the reported
due to gender, F(1, 100) ⫽ 0.07, p ⫽ .79 or to task order, F(3, group by self condition by emotion condition interaction effect
100) ⫽ 1.59, p ⫽ .19. remained significant F(2, 110) ⫽ 10.7, p ⬍ .00 when covariates
Group by self by emotion interaction. A significant group were included in the model. There were no main effects or inter-
by self condition by emotion condition interaction showed activa- actions due to task order, F(3, 105) ⫽ 1.68, p ⫽ .18, or to gender,
tion differences in several large clusters in mid parietal and pre- F(1, 105) ⫽ 0.22, p ⫽ .63.
frontal cortex areas, F(4, 696) ⫽ 25.51–22.7, p ⬍ .01. Follow-up
contrasts reported in Table 2 revealed that HS depressed youth Neuroimaging Results Covarying for
showed lower activity in both mid parietal and prefrontal areas
Depression Severity
when recognizing their self-happy face versus identifying another
adolescent’s happy face compared to LS depressed youth, who in Group by self interaction with depression severity covariage.
turn had less activity than HC youth. A unique group by self condition interaction emerged (see Table
Figure 4 shows that HS youth showed lower activity in MCS 3). Follow-up analyses showed that HC exhibited similar activity
clusters composed by the medial prefrontal cortex (BA10), a to self and other faces in the left cerebellum, bilateral precuneus,
canonical self-processing area (Sugiura et al., 2005), and a mid- and PCC as well as in the bilateral ACC (BA 32) and MFPC
parietal cluster composed by the parahippocampus, hippocampus, (BA10) areas. In contrast, LS depressed youth exhibited higher
and amygdala, t(1,696) ⫽ 5.28 – 4.67, p ⫽ .004 – 0.06, during activity in these areas for the self compared to other faces, whereas
happy self-faces versus happy other-faces. Notably, differences HS depressed youth demonstrated lower activity in these regions
were due both to significantly lower activity in response to the for the self-faces and higher activity for other-faces (see Figure 5).
happy self-faces and to significantly higher activity in response to Analyses of the extracted activity for the precuneus and PCC,
the happy other-faces in HS versus LS versus HC, which was bilateral ACC, and MPFC in SPSS confirmed the group by self
unique to this emotion. No group by self interaction effects interaction, F(2, 464) ⫽ 9.39, p ⫽ .00. However these analyses
emerged for either sad or neutral faces in the follow-up t tests. also yielded a brain region by self condition by group interaction,
However, when depression severity was included as a covariate in F(4, 464) ⫽ 2.64, p ⫽ .04, because of the fact that for the self-face
NEUROBIOLOGY SELF-FACE SUICIDAL YOUTH 9
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Figure 3. Depressed youth show higher dorsolateral prefrontal cortex (DLPFC) versus controls during all
conditions. High suicidality youth showed higher bilateral occipital and cuneus activities versus depressed low
suicidality and healthy controls during all conditions. See the online article for the color version of this figure.
Figure 4. High suicidality youth show lower activity than low suicidality depressed youth who in turn show
lower activity than healthy controls in limbic and medial prefrontal cortex (BA10) a canonical self-processing
area, during the self-face and higher activity during the other-face condition for happy faces. See the online
article for the color version of this figure.
existing knowledge of neurobiological correlates of self-referential fusiform cortex activity is thought to be linked to increased per-
processing among suicidal youth. sonal salience of stimuli (Gauthier, Tarr, Anderson, Skudlarski, &
Gore, 1999). In a similar vein, self-face processing has been linked
Right Lateral Cortical Structures and Self Processing to increased occipital activation relative to recognition of others’
Identifying self-faces elicited greater recruitment of the right faces (Morita et al., 2008), and occipital regions tend to activate
occipital, fusiform, precuneus, and thalamus regions relative to more robustly when morphed faces have more self-relevant facial
identifying others’ faces, regardless of group or emotional valence, features than characteristics of others (Uddin et al., 2005). Simi-
even after controlling for depression severity. These areas repre- larly, the precuneus is reliably activated by self-related informa-
sent regions typically involved in face processing and general tion, including self-descriptive words and self-faces (Kircher et al.,
processing of self-related information. Higher fusiform activation 2000; Northoff et al., 2006). Finally, the observed thalamus activ-
has been shown to be involved in the neurobiology of face pro- ity in response to self-faces is consistent with past postulations
cessing, including self-faces (Kircher et al., 2000; Platek et al., suggesting that recruitment in this region is involved when eval-
2006; Platek, Wathne, Tierney, & Thomson, 2008), and greater uating mental representations of the self and emotional states
Table 3
Neural Areas That Distinguish High Suicidality vs. Low Suicidality Depressed vs. Healthy
Control Youth During Self and Other Processing When Severity of Depression is Included as
a Covariate
MNI
Interaction: Group by Self and Other Cluster
Condition size (K) p(K) Hemisphere x y z F p
Cerebellum Anterior Lobe, Culmen 379 .000 Left ⫺22 ⫺42 ⫺26 11.49 .349
Precuneus, Posterior Cingulate, BA 31 135 .000 Left and Right 4 ⫺56 28 9.21 .938
Anterior Cingulate and MPFC, BA 32, 10 696 .000 Left and Right ⫺2 54 ⫺2 9.07 .955
Note. The effects of group and self on the reported areas in Table 2 were also significant and present when
severity of depression was used as a covariate.
NEUROBIOLOGY SELF-FACE SUICIDAL YOUTH 11
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Figure 5. Healthy controls show similar activity in midline cortical structures (MCS) and cerebellum for self-
and other-faces, but depressed youth with low suicidality show lower MCS activity to other- versus self-faces,
whereas depressed youth with high suicidality showed lower MCS activity to the self- (particularly BA10 and
ACC) relative to other-faces. See the online article for the color version of this figure.
(Seger, Stone, & Keenan, 2004). Altogether, our results provide cognitive and social processes in highly suicidal depressed youth;
additional support that self-faces, regardless of affective valence, this is a hypothesis that deserves future inquiry and assessment. Of
have unique motivational value and elicit different neurophysio- note, our findings showed that heightened neural activity in the
logical processes than others’ faces. frontal inferior gyri region and visual cortex held even after
controlling for depression severity, providing further support that
Suicidality, Depression, and the Neurobiology hyperactivity in these regions is linked to high levels of suicidality
of Face Processing above and beyond the effects of depression.
(supported by MPFC, BA10) such as awareness and associative during processing of any self-relevant stimuli regardless of emo-
thinking regarding positive self-relevant cues (Kircher et al., 2001; tional valence, aberrant neural functioning in the MCS may be a
Kreplin & Fairclough, 2015), which together may in turn disrupt predictor of suicidality for youth above and beyond the effects of
preferential processing for the self and positive self-information severity of depression.
that is typical in healthy individuals (Ma & Han, 2010). Finally, These findings build on prior studies that demonstrate that
prior research has shown that depressive disorders are linked to depression and suicidality are linked to MPFC and limbic hypo-
poor recall of positive autobiographical memories (Haque, Juliana, activity in response to happy emotional faces (Henderson et al.,
Khan, & Hasking, 2014; Young, Bellgowan, Bodurka, & Drevets, 2014; Pan et al., 2013). Given that MPFC activity enables reward
2013). Quevedo et al. (2016) also found that depressed youth in motivated planning (Gerlach, Spreng, Madore, & Schacter, 2014;
this sample (with no comorbid PTSD) showed reduced activity in Pochon et al., 2002), suicidal youth might be more likely to fail to
a right midtemporal limbic cluster for happy self versus other integrate rewarding self-relevant experiences toward future behav-
faces. Thus, low levels of hippocampal and parahippocampal ior (Auerbach, Millner, Stewart, & Esposito, 2015), thereby further
activity during happy self faces in this study (and hyperactivity increasing suicide risk in these adolescents. Future research needs
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during other’s happy faces) might reflect deficient encoding and to elucidate whether impaired reward-motivated behavior is asso-
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retrieval of positive self-relevant cues in depressed, suicidal youth. ciated with lower limbic and MPFC function during positive-self-
Assuming that the current findings replicate, they may suggest that referential information.
the neurophysiology of encoding and retrieving rewarding per-
sonal information is uniquely disrupted because of high suicidality
Self-Referential Processing of Negative Self-Faces
in depressed youth.
and Suicidality
Counter to prediction, PCC, precuneus, and ACC activity for
happy self versus other faces did not differ among HS, LS, and HC Contrary to our hypotheses, we found no group by self condition
groups prior to controlling for depression severity. In addition to interaction effects on neural function during sad or neutral face
self-processing, the ACC and PCC have been implicated in emo- recognition, both before and after controlling for depression se-
tion regulation and cognitive control, conflict monitoring, making verity. These results conflict with prior findings showing that
evaluative judgments, and social cognition (Brewer, Garrison, & depression and suicidality are associated with limbic hyperactiva-
Whitfield-Gabrieli, 2013; Lee & Siegle, 2012), which prior studies tion to negative stimuli, including negative emotional faces (Hen-
have implicated in responses to both positive and negative self- derson et al., 2014; Thomas et al., 2011). However, the tasks
information among depressed individuals, or individuals with adopted in prior research entailed emotion perception or facial
greater negative affect (Lemogne et al., 2009; Nejad et al., 2013). emotion discrimination of unfamiliar faces (e.g., matching facial
Given that the ACC and PCC are thought to be involved in a expressions, identifying facial emotions), which contrast the de-
number of cognitive and emotional functions relevant to self- mands of the task adopted in the current investigation, which
processing, it is possible that such functions did not differ during required participants to discriminate between self- versus other-
emotionally charged self- processing between the groups studied faces. Thus, it is possible that our task demands primarily elicited
here. Future work needs to elucidate unique self-processes differ- recruitment of neural networks involved in self-processing, which
entially supported by MPFC and BA10 versus ACC or PCC across may have contributed to a different pattern of results among
emotional conditions to frame these findings. suicidal youth. An alternative explanation for our own lack of
Interestingly, after controlling for depression severity, results findings for negative self-faces versus other-faces across diagnos-
showed that HS youth differed from LS youth in neural activation tic groups is that depressed individuals, or individuals at higher
during self versus other faces recognition across all emotions in risk for suicide, may be more likely to exhibit hyperactivity in
MCS (ACC, PCC, precuneus, and BA10) and the cerebellum, brain areas involved in emotional and self-referential processing
whereas the effect of suicidality on midtemporal limbic areas (i.e., even at baseline, as suggested by prior research showing neural
the hippocampus, parahippocampus, and amygdala) during the hyperactivation across many different task conditions (Nejad et al.,
processing of happy self versus other faces was reduced to non- 2013). Therefore, it may be more challenging to find differences
significance. In other words, limbic reactivity to emotionally when comparing neural response to negative self-referential infor-
charged self-information no longer distinguished depressed HS mation versus other information, given that both conditions might
youth from LS youth once the severity of depressive symptoms elicit higher levels of activity in relevant brain areas. Finally, all
were controlled. Instead, suicidality was associated with distinct participants were more accurate for identifying happy self-faces,
neural patterns within MCS areas in response to self versus other suggesting that happy self faces are more emotionally salient and
faces, irrespective of emotional valence (particularly low BA10 easier to recognize.
activity) for self faces. Altogether, these findings suggest that
suicidality is indeed associated with atypical neural activity in
Limitations
response to self-information. Youth with more severe suicidality
and depressive symptoms exhibit blunted neural response to pos- Despite the number of strengths inherent in the current study,
itively valenced self-referential stimuli, particularly in areas asso- such as the use of a rigorous research design, a large sample size,
ciated with mood and emotional memory (limbic areas), consistent an adolescent sample, and a novel task, this investigation also has
with a number of studies documenting diminished saliency of and some limitations to note. First, most of the high suicidality ado-
memory for processing (including less encoding and retrieval) lescents were recruited from a different site (Mpls site) than youth
positive self-information among depressed individuals (Stuhrmann in other diagnostic groups, and thus the effects of scanning site
et al., 2011; Yoshimura et al., 2014).Results further suggest that cannot be entirely decoupled from the effects of suicidality, par-
NEUROBIOLOGY SELF-FACE SUICIDAL YOUTH 13
ticularly for findings involving the occipital and cuneus activity. enfeld et al., 2009). Research suggests that suicide attempters are
However, analyzing only Mpls data in SPM8 yielded similar deficient in these executive functions, leading to greater impulsiv-
effects to those found for the whole sample, and main effects of ity and poor problem solving that increase suicide attempt risk
group and group by condition interactions remained significant (Annweiler et al., 2013). Thus, overlap in neural circuitry (i.e.,
when controlling for scanning site. Second, although prior research MCS) involved in both automatic self-referential processing and
has found RT differences during self-referential or emotional face executive function might help explain why depressed youth with
processing tasks between groups at higher risk for suicide (e.g., disturbed self-schemas are more likely to engage in suicidal acts.
depressed individuals) and low risk/psychologically healthy In order to further explore this possibility, future research should
groups, we did not find differences in accuracy or RT among carefully investigate how MCS function during self-referential
clinical groups in this study. Thus, it is possible that our task may processing of emotional information is associated with distinct
be lower in cognitive demand or difficulty level, and that our aspects of suicidality, such as unplanned/impulsive suicide at-
neuroimaging findings should be interpreted with this concern in tempts versus planned suicide attempts or suicidal ideation in both
mind. However, it should be noted that the lack of behavioral adults and young patients. This research may potentially help
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findings is likely due to important methodological differences in identify targets for suicide interventions, such as more effective
This document is copyrighted by the American Psychological Association or one of its allied publishers.
this study, notably that the task was deliberately designed to cognitive control strategies that could be used in response to
enhance identification accuracy of emotional self- and other- emo- self-relevant emotional information.
tional faces and to reduce variation in accuracy by eliminating Our findings also emphasize the importance for future research
more ambiguous faces (e.g., faces with 40%– 60% self features) to examine the neural underpinnings of biased self-processing
and by using clear emotional expressions in all presented images. among suicidal youth with and without depression. We focused on
This was to ensure that any neural differences detected were not
suicidality among clinically depressed youth given the alarming
confounded by misidentification of self versus other faces or of
rates of suicidal behavior and completed suicides among this
emotion type. Thus, similar RTs and accuracy across groups
group. However, the highly suicidal group also had more severe
suggest that the task is equally feasible for high suicidal, low
depressive symptoms, suggesting the possibility that aberrant neu-
suicidal, and control youth, and likely valid for other psychiatri-
ral response to positively valenced self-related information and
cally disordered populations. It is also important to note that this is
self cues in general may be associated with severe depression,
the first study to examine self-referential processing among de-
which may in turn contribute to or be associated with higher
pressed, suicidal youth using both positive and negative self- and
other-faces. In order to better understand how emotionally charged suicidality. Longitudinal and cross-diagnostic research is needed to
self-processing may relate to suicide, it will be essential to use a test this hypothesis. In addition, it is important to recognize that
variety of tasks in future research that can assess multiple aspects suicidality is a transdiagnostic behavior that is also observed
of self-referential processing, such as attention, perception, iden- among youth with many other forms of psychopathology. When
tification, and recall of emotional self-referential stimuli. depression severity effects were controlled, findings strongly sug-
gested that neural activity in MCS regions were particularly pre-
dictive of more severe suicidality. Along these lines, previous
Conclusions and Direction for Future Research research with this same sample by Quevedo et al. (2016) found that
In sum, the current findings suggest atypical neural functioning although nonmaltreated depressed youth also exhibited altered
among suicidal, depressed youth, particularly blunted emotional midtemporal limbic activity (hippocampus, parahippocampus, and
reactivity and awareness in response to positively valenced self- amygdala) to positively valenced self-stimuli, they did not show
faces and self-faces in general. These findings advance knowledge blunted activity in MPFC (specifically BA10) observed among
regarding the neural correlates of suicidality during adolescence, depressed suicidal youth in this study, in analyses with and without
when vulnerability to suicide is especially high. Moreover, these severity as a covariate. This suggests that suicidal youth with a past
neural findings are consistent with existing evidence that de- history of maltreatment may be especially likely to exhibit disrup-
pressed youth with high suicidality, compared to depressed youth tions in the higher order cognitive processing of self-relevant
with low suicidality, may have more negative or disturbed self- information supported by MPFC/BA10 or that functional abnor-
schemas that influence the automatic information processing of malities in these areas are common to both suicidal, severely
emotionally charged self-information (Burke et al., 2016). Thus, depressed, and maltreated youth. Future research examining links
findings suggest the possibility that dysfunctional processing of amomg suicidality, child maltreatment, and disrupted MCS during
emotional self-related information, particularly that of positive self-processing is thus warranted. Finally, it will be important for
valence, may contribute to increased risk for suicide among de- future research to focus on MCS areas to understand how disturbed
pressed youth. Findings from this study are also consistent with self-processing may predict suicide risks across diagnostic groups.
research showing that suicide attempters have more impaired
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