Electrocortical Processing of Social Signals of Threat in Combat-Related Post-Traumatic Stress Disorder

Biological Psychology 94 (2013) 441–449

Contents lists available at ScienceDirect

Biological Psychology

journal homepage: www.elsevier.com/locate/biopsycho

Electrocortical processing of social signals of threat in combat-related post-traumatic stress disorder

a,∗ a a,c

Annmarie MacNamara , David Post , Amy E. Kennedy ,

b a,b,c

Christine A. Rabinak , K. Luan Phan

Department of Psychiatry, University of Illinois at Chicago, United States

Department of Psychiatry, University of Michigan, United States

Mental Health Service Line, Jesse Brown VA Medical Center, United States

a r t i c l e i n f o a b s t r a c t

Article history: Post-traumatic stress disorder (PTSD) is characterized by avoidance, emotional numbing, increased

Received 21 March 2013

arousal and hypervigilance for threat following a trauma. Thirty-three veterans (19 with PTSD, 14 without

Accepted 30 August 2013

PTSD) who had experienced combat trauma while on deployment in Iraq and/or Afghanistan completed

Available online 8 September 2013

an emotional faces matching task while electroencephalography was recorded. Vertex positive poten-

tials (VPPs) elicited by happy, angry and fearful faces were smaller in veterans with versus without

Keywords:

PTSD. In addition, veterans with PTSD exhibited smaller late positive potentials (LPPs) to angry faces

PTSD

and greater intrusive symptoms predicted smaller LPPs to fearful faces in the PTSD group. Veterans with

Numbing

PTSD were also less accurate at identifying angry faces, and accuracy decreased in the PTSD group as

Vertex positive potential

VPP hyperarousal symptoms increased. These ﬁndings show reduced early processing of emotional faces,

Late positive potential irrespective of valence, and blunted prolonged processing of social signals of threat in conjunction with

LPP impaired perception for angry faces in PTSD.

Emotional faces

1. Introduction work have led to a substantial platform of knowledge about emo-

tional brain responses in PTSD (Nemeroff et al., 2006; Pitman et al.,

Post-traumatic stress disorder (PTSD) is a debilitating men- 2012), several inconsistent results have also emerged, thus raising

tal disorder that results following exposure to a traumatic event questions about key biological dimensions of the disorder (Lanius,

such as armed combat, motor vehicle accident or sexual assault Bluhm, Lanius, & Pain, 2006; Lanius, Brand, Vermetten, Frewen, &

(American Psychiatric Association, 2000). Patients with PTSD expe- Spiegel, 2012).

rience intense emotional reactions when reminded of their trauma Many affective neuroimaging studies in PTSD have focused on

and report exaggerated arousal (e.g., being easily startled), both the early, automatic processing of threatening stimuli as reﬂected

of which suggest emotional hyper-responsivity. However, individ- in amygdala activity. To this end, researchers have used masked

uals with PTSD also report anhedonia and a decreased capacity (Rauch et al., 2000) or brieﬂy presented (e.g., 200 ms; Shin et al.,

for emotion (‘emotional numbing’), suggesting emotional hypo- 2005) pictures or words. Pictorial stimuli are often faces, with

responsivity. Characterizing the neural basis of these diverse fearful faces representing indirect or ambiguous threat and angry

emotional responses poses a major challenge to contemporary faces representing direct or non-ambiguous threat (Kim et al.,

psychiatric research (Friedman, Resick, Bryant, & Brewin, 2011). 2011). Other work has used images from the International Affective

Functional neuroimaging techniques have focused primarily on Picture System (IAPS; Lang, Bradley, & Cuthbert, 2005), or trauma-

the study of brain function related to fear perception in exam- speciﬁc stimuli (e.g., traumatic scripts, combat images; Rauch et al.,

ining emotional responsivity. While consistent ﬁndings from this 1996; Shin et al., 1997). Evidence of increased amygdala response

to threatening stimuli in PTSD has been observed in some (Rauch

et al., 1996, 2000; Shin et al., 1997, 2005) but not all of these stud-

ies (Bremner et al., 1999; Britton, Phan, Taylor, Fig, & Liberzon,

∗

Corresponding author at: Department of Psychiatry, University of Illinois at

2005; Lanius et al., 2002; Phan, Britton, Taylor, Fig, & Liberzon,

Chicago, 1747 West Roosevelt Road, Chicago, IL 60607, United States.

2006; Sakamoto et al., 2005; Shin et al., 1999). Indeed, recent meta-

Tel.: +1 312 413 4707.

analyses (Etkin & Wager, 2007; Hayes, Hayes, & Mikedis, 2012;

E-mail addresses: [email protected],

[email protected] (A. MacNamara). Lanius et al., 2006; Simmons & Matthews, 2012) have questioned

442 A. MacNamara et al. / Biological Psychology 94 (2013) 441–449

the consistency of amygdala hyper-reactivity in PTSD. Importantly, Wager, 2007; Hayes et al., 2012; Lanius et al., 2006; Simmons &

the tendency for increased amygdala activity in PTSD to have been Matthews, 2012).

more reliably observed in response to masked or brieﬂy-presented As an early measure of face-processing, the vertex positive

stimuli (Bryant et al., 2008; Felmingham et al., 2010; Rauch et al., potential (VPP) is a positive-going ERP component that peaks

2000; Shin et al., 2005) suggests that it may reﬂect an automatic at central sites within 200 ms following stimulus onset and is

arousal response (Lanius et al., 2006). larger for faces compared to other types of stimuli (e.g., Bentin

Differences in stimuli may partially explain discrepancies et al., 2007; Rossion & Jacques, 2008; Wheatley, Weinberg, Looser,

observed in prior work. For instance, increased reactivity to Moran, & Hajcak, 2011). The VPP is believed to reﬂect the perceptual

emotional stimuli in PTSD may be primarily observed for trauma- and structural encoding of faces (Carmel & Bentin, 2002; Jeffreys,

speciﬁc stimuli (e.g., personalized scripted imagery of trauma), 1989; Wheatley et al., 2011); moreover, the VPP responds to the

whereas decreased or normative reactivity may be more fre- emotional salience of faces, and may be especially enhanced to

quently observed for generic threat depictions (e.g., threatening threatening faces (Batty & Taylor, 2003; Blau, Maurer, Tottenham,

faces; Casada, Amdur, Larsen, & Liberzon, 1998; Pineles, Shipherd, & McCandliss, 2007; Righart & de Gelder, 2008).

Mostouﬁ, Abramovitz, & Yovel, 2009). Combat-related PTSD, in The late positive potential (LPP) is distinguished by its abil-

particular, has been associated with reduced response when ity to measure the sustained, elaborative processing of stimulus

processing non-traumatic threatening/aversive stimuli (Armony, salience (Cuthbert, Schupp, Bradley, Birbaumer, & Lang, 2000). The

Corbo, Clément, & Brunet, 2005; Phan et al., 2006). Additionally, LPP is a centro-parietal, positive-going ERP component that begins

the type of ‘control’ stimuli that are used may impact results: approximately 300 ms after stimulus onset and is larger for emo-

for example, among studies that use facial stimuli to evaluate tional compared to neutral stimuli (Foti, Hajcak, & Dien, 2009;

threat-processing in PTSD, neutral faces may not provide the MacNamara, Foti, & Hajcak, 2009; Schupp et al., 2000). In addition

most appropriate comparison, because anxious individuals may to tracking the affective nature of stimuli, the LPP is also sensi-

interpret even these baseline stimuli differently than non-anxious tive to individual differences in the perceived salience of stimuli.

individuals (Cooney, Atlas, Joormann, Eugène, & Gotlib, 2006; For instance, the LPP is larger for photographs of relatives, or one’s

Somerville, Kim, Johnstone, Alexander, & Whalen, 2004). Differ- own name or face (Grasso & Simons, 2011; Tacikowski & Nowicka,

ences in the types of control groups employed (i.e., trauma-exposed 2010) and the LPP elicited by pictures of food is larger in individuals

versus non-exposed controls) may also add to the heterogeneity of who have been food-deprived (Stockburger, Schmälzle, Flaisch,

ﬁndings in PTSD. Bublatzky, & Schupp, 2009). The LPP is also sensitive to more willful

In addition to hemodynamic measures, event-related potentials modulations of stimulus salience. For example, the LPP is smaller

(ERPs) can be used to measure affective processing in PTSD. ERPs when participants are asked to reduce the emotional salience of

have excellent temporal resolution, and can therefore be used to affective pictures (Hajcak & Nieuwenhuis, 2006; Moser, Hajcak,

examine both early and late (i.e. prolonged) threat processing in Bukay, & Simons, 2006; Parvaz, MacNamara, Goldstein, & Hajcak,

the same experimental paradigm. In addition, because ERPs do not 2012). Therefore, the LPP seems to be sensitive to both bottom-up

rely on the ‘subtraction’ analysis used in typical functional mag- (i.e., content-driven) and top-down (i.e., strategic) modulations of

netic resonance imaging (fMRI) contrast images; group differences stimulus salience, and may be an excellent tool for investigating

in neural response to threatening stimuli can be more easily dis- the elaborated processing of threatening stimuli in PTSD.

tinguished from differences in response to control stimuli. Most The current study used the VPP and the LPP to examine the

commonly, ERPs have been used to examine abnormalities in the processing of emotional stimuli in a group of returning veterans

processing of non-affective target stimuli and affective distracter with and without PTSD. Given high levels of interpersonal dys-

stimuli in PTSD (Karl, Malta, & Maercker, 2006). Few studies, how- function in combat-related PTSD (Frueh, Turner, Beidel, & Cahill,

ever, have utilized ERPs to examine the processing of task-relevant, 2001; Jordan et al., 1992; Ruscio, Weathers, King, & King, 2002),

emotional stimuli in PTSD. we used facial stimuli presented in the context of an affect match-

In one of these studies, Felmingham, Bryant, and Gordon (2003) ing task (Hariri, Tessitore, Mattay, Fera, & Weinberger, 2002; Phan

showed an angry and a neutral face to individuals with PTSD et al., 2008). We expected to observe evidence of altered threat-

and a group of controls while electroencephalography (EEG) was processing in PTSD for the LPP (Tso, Chiu, King-Casas, & Deldin,

recorded. Pictures were shown repeatedly for 110 ms in a pas- 2011), however, based on conﬂicting prior results (Armony et al.,

sive viewing task, and the authors used negative-going ERPs to 2005; Etkin & Wager, 2007; Grasso & Simons, 2012; Hayes et al.,

measure the processing of facial stimuli. Results revealed that 2012; Lanius et al., 2006; Simmons & Matthews, 2012), we did not

individuals in the control group evinced larger temporo-occipital have directional hypotheses for the ERPs. Based on prior work, we

negativities around 100 ms and 650 ms after picture onset, for thought it possible that we would observe either increased ampli-

angry compared to neutral faces. Individuals in the PTSD group did tudes to threatening stimuli, reﬂecting hypervigilance (Karl et al.,

not show this difference for angry versus neutral faces, indicating 2006; Shin et al., 2005) or decreased amplitudes, possibly reﬂect-

reduced discrimination between neutral and threatening stimuli. ing avoidance or numbing symptoms (Felmingham et al., 2003;

Unfortunately, Felmingham et al. (2003) did not include other face Felmingham, Bryant, Kendall, & Gordon, 2002). Behaviorally, we

types, so it could not be determined whether PTSD-related deﬁcits expected to observe reduced accuracy for individuals with PTSD

in emotion-processing were speciﬁc to threatening faces. More- – especially for trials containing threatening expressions (Pollak,

over, pictures were presented for only 110 ms and the sustained Cicchetti, Hornung, & Reed, 2000; Shenk, Putnam, & Noll, 2012).

processing of threatening pictures, which might have indicated dif-

ferences between conditions for the PTSD group, was not examined.

2. Method

Brieﬂy displayed images may reveal ‘bottom-up’ hyperreactiv-

ity often reported by patients with PTSD (Etkin & Wager, 2007),

2.1. Participants

whereas longer stimulus presentation durations may be neces-

sary to investigate ‘top-down’ processes (e.g., emotion regulation Participant demographics, symptomatology and comorbid diagnoses are pre-

sented in Table 1. Participants were 33 combat-exposed male veterans who had

deﬁcits, avoidance) that may contribute to the pathophysiology of

returned from deployment in Operation Enduring Freedom or Operation Iraqi Free-

PTSD (Felmingham et al., 2008; Frewen & Lanius, 2006). Moreover,

dom (OEF/OIF). Participants were recruited from the Veterans Affairs (VA) Ann

an examination of both early and late threat-processing in PTSD

Arbor Healthcare System, as well as from the surrounding community via paper

could help resolve prior discrepancies in the literature (Etkin & advertisements and posted ﬂyers.

A. MacNamara et al. / Biological Psychology 94 (2013) 441–449 443

Table 1

Participant demographics. Top section: means (and standard deviations) for age, years of education and symptomatology. Bottom section: ethnicity and comorbid diagnosis

by number and percentage of participants.

CEC PTSD Group comparison

n = 14 n = 19

Age 34.71 (8.80) 29.95 (8.03) ns

Years of education 15.64 (1.50) 12.89 (1.33) p < 0.001

CAPS total 3.43 (4.42) 72.79 (14.34) p < 0.001

Re-experiencing 0.43 (1.09) 18.11 (6.79) p < 0.001

Avoidance 1.36 (1.98) 27.37 (7.16) p < 0.001

Hyperarousal 1.64 (2.56) 27.32 (4.35) p < 0.001

PCL-M 24.93 (11.69) 56.21 (10.52) p < 0.001

CES 21.64 (5.37) 24.21 (7.30) ns

Ham-D 1.36 (1.95) 12.74 (3.23) p < 0.001

Ethnicity n % n %

Caucasian 12 85.70 19 100.0 ns

Other 2 14.30 – –

Comorbid diagnoses

MDD – – 4 21.0 ns

Alcohol abuse – – 3 15.8 ns

Group comparisons were performed using independent t-tests, except for ethnicity and comorbidity comparisons, which were performed using Fisher’s Exact Test to account

for low cell counts. ns = non-signiﬁcant.

The Structured Clinical Interview for the Diagnostic and Statistical Manual of screen. Face-matching trials could be fearful, angry or happy. On shape-matching

Mental Disorders IV (SCID-I/NP for DSM-IV, First, Spitzer, Gibbon, & Williams, 1995) trials, participants were instructed to choose the shape at the bottom of the screen

was used to assess for past and present psychological disorders; PTSD sympto- that matched (i.e., had the same form as) the target shape at the top of the screen.

matology and severity was also measured using the Clinician Administered PTSD In line with previous EFT studies (e.g., Labuschagne et al., 2010; Phan et al., 2008)

Scale (CAPS; Blake et al., 1995) and the PTSD-Checklist, military version (PCL- we used geometric shapes as control stimuli instead of neutral faces, because neu-

M; Blanchard, Jones-Alexander, Buckley, & Forenia, 1996). Combat exposure was tral faces may be more inﬂuenced by individual differences (e.g., anxiety levels;

assessed using the Combat Exposure Scale (CES; Keane et al., 1989). Somerville et al., 2004).

Participants were eligible for the PTSD group (n = 19) if they met current crite- The task was divided into two blocks, with each block having 12 angry, 12

ria for combat-related PTSD and had scores of at least a 40 or greater on the CAPS, fearful, 12 happy and 12 shape-matching trials; trials were presented randomly

reﬂecting moderate to severe PTSD symptoms. Comorbid Axis I disorders were per- within each block, for a total of 96 trials across both blocks. The inter-trial interval

mitted in the PTSD group, with the exception of current or prior psychosis or mania varied between 1000 and 3000 ms, during which time a white ﬁxation cross was

or hypomania (see Table 1). History of head trauma, loss of consciousness, and centrally presented on a black background. During presentation of the images, par-

traumatic brain injury (of any severity) were exclusionary criteria for all partici- ticipants were instructed to maintain focus on the screen, but were permitted to

pants. Participants were eligible to be in the combat-exposed control group (CEC; look freely at the images. Participants performed 6 practice trials prior to beginning

n = 14) if they did not meet criteria for PTSD or any other Axis I disorder (disorders the experiment, which used facial stimuli that were not used in the experiment.

>6 months prior were allowed and were asymptomatic for PTSD according to the

CAPS (scores <20). Compared to participants in the CEC group, those in the PTSD

2.4. EEG recording and data reduction

group had signiﬁcantly higher scores on the PCL-M (t(31) = 8.05, p < 0.001) and CAPS

(t(31) = 19.85, p < 0.001); participants in the CEC and PTSD groups did not differ on

Continuous EEG was recorded using an elastic cap and the ActiveTwo BioSemi

level of combat exposure (t(31) = 1.16, p > 0.25; see Table 1). Participants in the PTSD

system (BioSemi, Amsterdam, Netherlands). Thirty-four electrode sites (standard

group also reported greater levels of depression than participants in the CEC group

32 channel setup, as well as FCz and Iz) were used, based on the 10/20 system; in

(t(31) = 11.69, p < 0.001; see Table 1), as measured by the Hamilton Depression Rating

addition, one electrode was placed on each of the left and right mastoids. The elec-

Scale (Ham-D; Williams, 1988).

trooculogram (EOG) generated from eyeblinks and eye movements was recorded

None of the participants were taking psychiatric medications (at least 4 weeks

from four facial electrodes: vertical eye movements and blinks were measured with

prior to the EEG session) and none had signiﬁcant medical or neurological disorders.

two electrodes placed approximately 1 cm above and below the right eye; horizon-

All participants were paid for their time, and gave written informed consent, as

tal eye movements were measured using two electrodes placed approximately 1 cm

approved by the VA Ann Arbor Healthcare System Institutional Review Board.

beyond the outer edge of each eye. The EEG signal was pre-ampliﬁed at the electrode

to improve the signal-to-noise ratio. The data were digitized at 24-bit resolution

2.2. Materials with a Least Signiﬁcant Bit (LSB) value of 31.25 nV and a sampling rate of 1024 Hz,

using a low-pass ﬁfth order sinc ﬁlter with a −3 dB cutoff point at 208 Hz. The voltage

Twenty-four angry, 24 fearful and 24 happy faces were selected from the Gur from each active electrode was referenced online with respect to a common mode

emotional faces set (Gur et al., 2002); half of the faces depicted male actors and the sense active electrode producing a monopolar (non-differential) channel.

other half depicted female actors. In addition, 3 geometric shapes – a circle, a square

and a triangle – were used as control stimuli (see task description, below). The shapes

2.5. Data reduction and analysis

were presented in white on a black background; faces were presented in color on a

black background, on a 19 computer screen using Presentation software (Neurobe-

Off-line analyses were performed using Brain Vision Analyzer 2 software (Brain

havioral Systems, Inc., Albany, CA). Participants were seated approximately 60 cm

Products, Gilching, Germany). Data from correct trials were segmented for each

from the screen.

trial beginning 200 ms prior to picture onset and continuing for 3200 ms (3000 ms

beyond picture onset); baseline correction for each trial was performed using the

2.3. Task 200 ms prior to picture onset. Ofﬂine, data were re-referenced to the average of the

two mastoids and band-pass ﬁltered with high-pass and low-pass ﬁlters of 0.01 and

Participants completed a version of the Emotional Face-Matching Task (Hariri 30 Hz, respectively. Eye blink and ocular corrections used the method developed by

et al., 2002), which has proven useful in characterizing threat-processing in anxious Gratton, Coles, and Donchin (1983). Artifact analysis was used to identify a voltage

␮ ␮

and non-anxious participants (Labuschagne et al., 2010) and which would facilitate step of more than 50.0 V between sample points, a voltage difference of 300.0 V

comparison with prior ERP work in PTSD (Felmingham et al., 2003). On each trial, 3 within a trial, and a maximum voltage difference of less than 0.50 ␮V within 100 ms

◦ ◦

images (each subtending a visual angle of approximately 11 × 13 ) were presented intervals. Trials were also inspected visually for any remaining artifacts, and data

for 3000 ms, in a ‘triangular’ arrangement – i.e., one image was centered in the top- from individual channels containing artifacts were rejected on a trial-to-trial basis.

half of the screen and the other two images were presented in the bottom-half of For figures, a digital low-pass (12 Hz) filter was applied offline before plotting the

the screen (one to the left and one to the right). There were “face-matching” and waveforms; statistical analyses were conducted using the original ﬁlter settings.

“shape-matching” trials. The VPP was scored at fronto-central pooling, Fz, FC1, FC2, FCz and Cz (Foti, Olvet,

On each face-matching trial, the faces of three different actors were presented: Klein, & Hajcak, 2010). For each condition and participant, peak VPP amplitude was

two were always emotional and one always bore a neutral expression. Participants deﬁned as the local positive peak evident in the 150–300 ms period after stimulus

were instructed to select one of the faces at the bottom of the screen that bore the onset evident in the grand-average waveforms (Fig. 2). Of note, the search window

same emotional expression as the ‘target’ face centered in the top portion of the used for detection of VPP peak amplitudes was wider than in some previous studies,

444 A. MacNamara et al. / Biological Psychology 94 (2013) 441–449

Fig. 1. Bar graphs depicting reaction time (RT, ms; left) and accuracy (% correct; right) for participants in the CEC group (light bars) and the PTSD group (dark bars). Bars

represent standard error of the mean. Signiﬁcant differences using Tukey’s (or Tukey–Kramer’s) tests are indicated with horizontal brackets (all ps < 0.05).

Table 2

Means (and standard deviations) for VPP and LPP amplitudes elicited by emotional faces and shapes.

CEC PTSD Group comparison

Condition

VPP (␮V) Angry faces 9.39 (6.72) 1.91 (3.82) p < 0.05

Fearful faces 9.09 (5.51) 3.70 (3.44) p < 0.05

Happy faces 8.61 (5.60) 4.62 (4.44) p < 0.05

Shapes 7.64 (5.32) 5.76 (3.88) ns

LPP (␮V) Angry faces 4.89 (3.38) 1.55 (3.90) p < 0.05

Fearful faces 2.98 (3.87) 0.55 (4.76) ns

Happy faces 1.05 (3.81) 3.80 (6.12) ns

Shapes −2.37 (6.74) −1.65 (3.53) ns

Group comparisons were performed using Tukey–Kramer’s tests, except for the LPP elicited by angry and fearful faces, for which a priori comparisons were performed using

independent t-tests. ns = non-signiﬁcant.

in order to account for the later latency of VPPs elicited by shapes (Caldara et al., with faces elicited worse performance than trials with shapes

2003). After peak detection, mean amplitudes in a 20 ms window centered on peaks

and angry faces elicited the worst performance (i.e., shapes accu-

were extracted for statistical analysis. The LPP was scored by averaging amplitudes

racy > happy accuracy = fearful accuracy > angry accuracy; Tukey’s

at centro-parietal pooling, Cz, CP1, CP2 and Pz (MacNamara & Hajcak, 2010) from

1 p < 0.05). A near-signiﬁcant between-groups effect (F(1,31) = 4.15,

600 to 3000 ms after picture onset (Dennis & Hajcak, 2009; Foti et al., 2009).

= .

Accuracy data were computed as the total percentage of correct trials per con- p = 0.05, p 0 12) was qualiﬁed by an interaction between

dition. Reaction time was computed as the amount of time it took participants to 2

group × condition (F(1.41,43.55) = 4.49, p < 0.05, p = 0.13). Based

respond from picture onset, on correct trials only. Behavioral and ERP data were

on our a priori prediction that there would be group differences

analyzed using a 2 (group: CEC, PTSD) × 4 (condition: angry, fearful, happy, shapes)

for accuracy on trials with threatening faces, we performed

mixed measures analysis of variance (ANOVA). Signiﬁcant interactions were fol-

lowed up using independent t-tests for planned comparisons and Tukey’s test (or planned comparisons (using independent t-tests) to examine

Tukey–Kramer‘s test for unequal sample sizes) for unplanned comparisons/post hoc group differences for angry and fearful faces. Compared to the

tests (family-wise error rate was controlled at p < 0.05). Statistical analyses were per-

CEC group, the PTSD group were less accurate on trials with angry

formed using PASW (Version 18.0) General Linear Model software and Greenhouse

faces (t(31) = 2.55, p < 0.05); there was no group difference for

Geisser corrections were applied as necessary for violations of sphericity.

fearful faces (p > 0.73). Using post hoc Tukey–Kramer’s tests, there

were no group differences for trials containing happy faces or

3. Results shapes.

3.1. Behavioral

3.2. ERPs

Fig. 1 presents reaction time (left) and accuracy (right) data

for each condition, shown separately for each group. As is sug-

Table 2 presents mean VPP and LPP amplitudes for each condi-

gested by the ﬁgure, there was an effect of condition on reaction

2 tion and group.

time (F(2.12,68.56) = 181.62, p < 0.001, p = 0.85). Post hoc tests

indicated that trials with faces elicited slower RTs than trials

with shapes; angry faces elicited the slowest RTs (i.e., angry

RT > fearful RT = happy RT > shapes RT; Tukey’s p < 0.05). There was 3.2.1. VPP

no interaction between condition and group (p > 0.43) and no Fig. 2 presents grand-average amplitudes for each condition and

between-groups effect for reaction time (p > 0.94). group at the fronto-central pooling where the VPP was scored. Sta-

There was an effect of condition on accuracy tistical analysis of VPP amplitudes indicated that there was no main

(F(1.41,43.55) = 40.61, p < 0.001, p = 0.57), such that trials effect of condition on the VPP (p > 0.38). A signiﬁcant between-

groups effect (F(1,31) = 10.12, p < 0.01, p = 0.25; CEC > PTSD)

was qualiﬁed by a signiﬁcant group × condition interaction

= .

1 (F(2.26,70) = 6.01, p < 0.01, p 0 16). Follow-up Tukey–Kramer’s

We also analyzed the LPP by scoring it in three separate time windows

tests were used to examine this interaction: compared to the CEC

(600–1000 ms, 1000–2000 ms and 2000–3000 ms after stimulus onset) and includ-

ing the factor “time window” in the overall ANOVA; results were unchanged. group, the PTSD group evinced signiﬁcantly smaller VPPs for angry,

A. MacNamara et al. / Biological Psychology 94 (2013) 441–449 445

Fig. 2. Grand-average waveforms at the fronto-central pooling where the VPP was maximal, shown separately for each condition within the CEC (left) and the PTSD (right)

groups.

Fig. 3. Grand-average waveforms at the centro-parietal pooling where the LPP was maximal, shown separately for each condition within the CEC (left) and the PTSD (right)

groups.

fearful and happy faces (p < 0.05); there was no group difference for examine group differences for angry and fearful faces. Compared

the VPP elicited by shapes. to the CEC group, the PTSD group evinced smaller LPPs in response

to angry faces (t(31) = 2.56, p < 0.02); no group differences were

observed for the LPP elicited by fearful faces (t(31) = 1.56, p > 0.12).

3.2.2. LPP

Post hoc Tukey–Kramer’s tests revealed no group differences for

Fig. 3 depicts grand-average waveforms for each condition and

the LPP elicited by happy faces or shapes.

group at the centro-parietal pooling where the LPP was scored;

To determine whether group differences in ERP and behavioral

Fig. 4 depicts the topographic distribution of voltage differences

variables would survive after controlling for depressive comorbid-

for each face type minus shapes, from 600-3000 ms after stim-

ity, we re-ran all ANOVAs and follow-up tests after temporarily

ulus onset. There was a main effect of condition on the LPP

2 removing participants with comorbid major depressive disorder

(F(3,93) = 11.10, p < 0.001, p = 0.26). Follow-up tests indicated

(MDD; n = 4 in the PTSD group) (Gold et al., 2011). Results were

that the LPP was larger for angry, fearful and happy faces compared

unchanged.

to shapes (Tukey’s p < 0.05). There was no overall between-groups

effect on the LPP (p > 0.61), however there was a signiﬁcant interac-

2 3.3. Correlations

tion between group × condition (F(3,93) = 4.09, p < 0.01, p = 0.12).

Based on our a priori prediction that there would be group dif-

Correlations were performed to examine relationships between

ferences for the LPP elicited by threatening faces, we performed

ERPs, behavioral performance and clinical symptomatology ; Bon-

two-tailed planned comparisons (using independent t-tests) to

ferroni corrections were used to control for Type I error. Across

participants, larger LPPs to fearful faces were associated with

greater accuracy on trials with fearful faces (r(31) = 0.56, p < 0.001);

We also analyzed peak latencies for the VPP. A main effect of condition

(F(3,93) = 21.01, p < 0.001, p = 0.40) indicated that VPP latencies for shapes were

slower than those for angry, fearful and happy faces (Tukey’s p < 0.05). There was

no interaction between group condition (p > 0.81) and no overall effect of group To reduce the total number of correlations performed, correlations were not

(p > 0.17). performed for the condition “shapes”.

446 A. MacNamara et al. / Biological Psychology 94 (2013) 441–449

Fig. 4. Headmaps depicting the spatial distribution of voltage differences for emotional faces minus shapes, from 600 to 3000 ms after picture onset (during the LPP).

Headmaps are shown separately for angry faces (left column), fearful faces (middle column) and happy faces (right column) within the CEC group (top row) and the PTSD

group (bottom row). Electrodes where the LPP was maximal are indicated in black.

there were no other signiﬁcant correlations between ERPs and In line with the present results, prior fMRI work has failed to ﬁnd

behavioral performance (all ps > 0.07). threat-speciﬁc modulation of FFA activity in PTSD (Rauch et al.,

Because of group differences in symptomatology and because 2000). In the present study, the ﬁnding that VPPs were reduced for

of lack of range on clinical measures in the CEC group, correlations all face types in the PTSD group is consistent with ERP work sug-

with symptomatology were performed only for the PTSD group gesting that PTSD may be associated with impairments in stimulus

(Catani, Adenauer, Keil, Aichinger, & Neuner, 2009; Felmingham discrimination and attention more generally (i.e., even for non-

et al., 2002). After controlling for multiple correlations, greater threatening stimuli; Felmingham et al., 2002). Such impairments

scores on the intrusive subscale of the CAPS were associated might arise from high levels of chronic arousal in PTSD, which may

with smaller LPPs to fearful faces (r(17) = −0.56, p < 0.02). There reduce individuals’ ability to distinguish relevant and irrelevant

were no other signiﬁcant correlations between ERP variables and stimuli (Kolb, 1987).

PTSD symptomatology (all ps > 0.05) or self-reported depression The LPP results were in line with those of Felmingham et al.

(all ps > 0.24). (2003), who found that individuals with PTSD exhibited smaller

Total CAPS scores, as well as scores on the re-experiencing and early and mid-latency negative-going ERPs in response to angry

avoidance subscales of the CAPS did not correlate with accuracy versus neutral faces. Because we used fearful and happy faces as

(all ps > 0.09), however as scores on the hyperarousal subscale of well as angry faces, the present results provide further evidence

the CAPS increased, participants showed reduced accuracy on tri- of the threat-speciﬁcity of PTSD-related abnormalities in the elab-

als with angry faces (r(17) = −0.61, p < 0.01; ps for other face types orated processing of facial stimuli. The results also suggest that

>0.19). After correcting for multiple correlations, there were no PTSD-related reductions in threat-processing may persist across

other signiﬁcant correlations between behavior and PTSD sympto- time, lasting up to 3000 ms after picture onset. In other prior

matology (all ps > 0.03) or self-reported depression (all ps > 0.10). work, reduced threat modulation of the LPP was found for trau-

matized individuals with greater stress-response symptoms (Tso

4. Discussion et al., 2011). Magnetoencephalographic (MEG) work has also found

evidence of the reduced processing of aversive stimuli in PTSD

The current study set out to characterize the electrocortical (Adenauer et al., 2010; but see Catani et al., 2009).

processing of socio-emotional stimuli in combat-exposed indi- The LPP has been source-localized to the visual cortex (Keil et al.,

viduals with and without PTSD. Across participants, the LPP was 2002); similarly, fMRI work has related variation in the LPP to

larger for emotional faces (Foti et al., 2010; MacNamara, Schmidt, occipital, parietal and inferotermporal cortices (Sabatinelli, Lang,

Zelinsky, & Hajcak, 2012) compared to shapes, and participants Keil, & Bradley, 2007). Based on animal models, some have sug-

were slower and less accurate on trials depicting threat (i.e., angry gested that the LPP might reﬂect re-entrant projections from the

faces) (Keil, Moratti, Sabatinelli, Bradley, & Lang, 2005; Vuilleumier, amygdala to areas of the visual cortex (Lang & Bradley, 2010);

Armony, Driver, & Dolan, 2001; Weinberg & Hajcak, 2011). Com- bidirectional contributions from parietal and frontal cortices may

pared to individuals in the CEC group, individuals in the PTSD group also underlie the generation and maintenance of the LPP (Moratti,

evinced smaller VPPs to all face types and smaller LPPs in response Saugar, & Strange, 2011). Thus, in the current results, reduced

to angry faces (on correct trials). Individuals with PTSD also showed LPPs to angry faces in the PTSD group likely reﬂects attenuated

reduced accuracy in response to angry faces (Pollak et al., 2000; processing of these stimuli in posterior visual attention regions

Shenk et al., 2012). of the brain. The fact that threat-speciﬁc group differences were

The VPP is believed to originate in the fusiform gyrus (FFA; observed only for the LPP and not the VPP suggests a particular

Deffke et al., 2007; Rossion, Joyce, Cottrell, & Tarr, 2003) and likely deﬁcit in the prolonged (i.e. late), facilitated processing of these

indexes the structural encoding of faces (Carmel & Bentin, 2002). stimuli.

A. MacNamara et al. / Biological Psychology 94 (2013) 441–449 447

Reduced elaborated processing of angry faces in PTSD might from the analysis, group differences in levels of depression and psy-

indicate an adaptive response to threat that is perceived as unavoid- chiatric comorbidities are limitations of the current study (Kemp

able (Foa & Hearst-Ikeda, 1996). For instance, following exposure et al., 2007).

to uncontrollable, fear-inducing events, reduced processing of In conclusion, the primary ﬁnding of the present study was

threatening stimuli might prevent reactivation of traumatic mem- that combat veterans with PTSD show blunted neural processing

ories and inhibit emotional arousal (Foa & Hearst-Ikeda, 1996; Foa, of social signals of threat that co-occurs with impaired percep-

Riggs, & Gershuny, 1995; Kolb, 1987). While group differences were tion of angry faces. Moreover, the results highlight the importance

not evident for the LPP elicited by fearful faces, greater intrusive of examining sustained neural activity to facial stimuli in order

symptomatology predicted smaller LPPs to fearful faces. Thus, in to investigate threat-speciﬁc PTSD abnormalities, which were

line with numbing accounts of PTSD (see also Horowitz, 1986; van not found for the VPP. Overall, the results suggest that the LPP

der Kolk, 1987), reduced processing of fearful faces in PTSD may may provide a useful means of examining emotion-processing

operate in response to trauma-induced intrusive symptomatology. abnormalities in PTSD and encourage further electrophysiological

While the present study found evidence of reduced threat- investigation of the processing of social signals of threat in combat-

processing in PTSD, other work has found the opposite. In the ERP related PTSD.

literature, evidence of PTSD-related increases in threat-processing

has been observed primarily in target-detection studies in which Acknowledgements

threatening stimuli have been presented as distractors that partic-

ipants are asked to ignore (Attias, Bleich, Furman, & Zinger, 1996;

This material is based upon work supported by the Depart-

Attias, Bleich, & Gilat, 1996; Bleich, Attias, & Furman, 1996). In addi-

ment of Veterans Affairs, Veterans Health Administration, Ofﬁce of

tion, a number of fMRI studies have found evidence of the increased

Research and Development, Clinical Sciences Research and Devel-

processing of masked or brieﬂy presented threatening stimuli in

opment, and the Veterans Affairs Merit Review Program Award (K.

PTSD (e.g., Rauch et al., 1996, 2000; Shin et al., 1997, 2005). There-

Luan Phan). The authors would like to acknowledge the OEF/OIF

fore, one possibility is that the past and present results might be

veterans for their participation in this research study and more

understood in terms of divergent threat-processing in PTSD when

importantly for their dedication and service to the United States

images are presented under conditions of limited awareness or

of America.

competitive attention (resulting in enhanced threat-processing)

versus when threatening stimuli are processed with full aware-

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