Applied Neuropsychology: Adult

ISSN: 2327-9095 (Print) 2327-9109 (Online) Journal homepage: http://www.tandfonline.com/loi/hapn21

Differential neural activation when voluntarily

regulating emotions in service members with
chronic mild traumatic brain injury

Michael N. Dretsch, Thomas A. Daniel, Adam M. Goodman, Jeffrey S. Katz,

Thomas Denney, Gopikrishna Deshpande & Jennifer L. Robinson

To cite this article: Michael N. Dretsch, Thomas A. Daniel, Adam M. Goodman, Jeffrey S. Katz,
Thomas Denney, Gopikrishna Deshpande & Jennifer L. Robinson (2017): Differential neural
activation when voluntarily regulating emotions in service members with chronic mild traumatic
brain injury, Applied Neuropsychology: Adult, DOI: 10.1080/23279095.2017.1362406

To link to this article: http://dx.doi.org/10.1080/23279095.2017.1362406

Published online: 19 Sep 2017.

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 APPLIED NEUROPSYCHOLOGY: ADULT
https://doi.org/10.1080/23279095.2017.1362406

none defined

Differential neural activation when voluntarily regulating emotions in service

members with chronic mild traumatic brain injury
Michael N. Dretscha,b, Thomas A. Danielc, Adam M. Goodmanc, Jeffrey S. Katzc,d,e, Thomas Denneyc,d,e, Gopikrishna
Deshpandec,d,e and Jennifer L. Robinsonc,d,e
a
US Army Aeromedical Research Laboratory, Fort Rucker, Alabama, USA; bHuman Dimension Division, Headquarters Training and Doctrine
Command, Fort Eustis, Virginia, USA; cDepartment of Psychology, Auburn University, Auburn, Alabama, USA; dAuburn University MRI Research
Center, Department of Electrical & Computer Engineering, Auburn University, Auburn, Alabama, USA; eAlabama Advanced Imaging
Consortium, Auburn University and University of Alabama, Birmingham, Alabama, USA

ABSTRACT KEYWORDS
The objective of this study was to characterize the functional activation of the neural correlates of Attentional bias; emotional
Downloaded by [Australian Catholic University] at 04:54 23 September 2017

voluntary regulation of emotion in soldiers both with and without chronic mild traumatic brain regulation; FMRI; mild
injury (mTBI). Using functional magnetic resonance imaging (fMRI) and a battery of cognitive and traumatic brain injury;
psychological health measures, we assessed differences between active-duty U.S. soldiers with military; TBI
chronic mTBI (n ¼ 37) and without (Controls, n ¼ 35). Participants were instructed to maintain
(passively view), enhance, and suppress emotions associated with negative and neutral visual
stimuli. The mTBI group showed significantly greater clinical symptoms, but only a mild decrement
in attention. Group contrasts, while controlling for posttraumatic stress disorder (PTSD) symptoms,
revealed a differential neural activation pattern compared to controls, but only during the enhance
condition. Specifically, the mTBI group showed greater activation in the precentral gyrus,
postcentral gyrus, inferior parietal lobe, insula, and superior temporal gyrus. Finally, the effect of
PTSD symptoms during the enhance condition was associated with accentuated activation of the
frontal and limbic regions implicated in both emotion regulation and PTSD. Hyperactivation of
neural regions in the mTBI group during the enhance condition may reflect vigilance towards
negative contextual stimuli and/or poor strategy that might result in suboptimal allocation of
resources to regulate emotions.

Introduction evidence of PTSD being associated with disrupted

neurocircuitry underlying emotional regulation
Individuals who suffer from chronic mild traumatic
(Dretsch, Wood, et al., 2016; Linnman, Zeffiro, Pitman,
brain injury (mTBI) often report difficulties regulating
& Milad, 2011). Hence, a better understanding of the
their emotional responses in social and interpersonal
neural mechanisms of emotional regulation in a military
settings (McDonald, 2005; Osborne-Crowley &
mTBI population, while controlling for PTSD
McDonald, 2016). Emotional regulation difficulties are
symptoms, may provide insight for improving
supported empirically in both civilian and military
diagnostics and treatment outcomes.
TBI populations as evidenced by clinical symptoms
Emotional regulation is a core component of coping
and behavioral indices of emotional volatility,
when presented with stressful, emotionally salient, and
impulsivity, mood symptoms (e.g., anxiety), aggression,
unpredictable scenarios. When such emotional
and increased frustration (Dretsch, Blieberg, et al., 2015;
responses are persistently left unregulated, they can
Dretsch, Silverberg, & Iverson, 2015; Goswami et al.,
result in chronic stress, which has been linked with a
2015; van der Horn, Liemburg, Scheenen, et al., 2016).
myriad of physical and psychological health symptoms
However, in military populations, the high comorbidity
(Boscarino, 2004). Compromised ability to regulate
between mTBI and psychological health conditions
emotional states may contribute to persistent somato-
such as posttraumatic stress disorder (PTSD) often
sensory (e.g., hearing), cognitive (e.g., concentration),
complicates clinician assessment of symptom etiology
and affective (e.g., depression) neurobehavioral
(Dretsch, Blieberg, et al., 2015; Dretsch, Williams,
symptoms prevalent in service members with chronic
et al., 2016). With high rates of comorbid PTSD,
mTBI (Dretsch, Blieberg, et al., 2015; van der Horn,
understanding military mTBI is complicated by the

CONTACT Michael Dretsch dretschphd@gmail.com Human Dimension Division, HQ, TRADOC, 950 Jefferson Ave, Fort Eustis, VA 23604, USA.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/hapn.
© 2017 Taylor & Francis Group, LLC
 2 M. N. DRETSCH ET AL.
Liemburg, Aleman, Spikman, & van der Naalt, 2016;
van der Horn, Liemburg, Scheenen, et al., 2016). As
such, it is important to assess the neural correlates of
voluntary emotional regulation in this population.
Regulation of emotion is a complex process in that it
implicates neuropsychological functions from multiple
cortical and subcortical regions and networks (for
reviews see Buhle et al., 2014; Kohn et al., 2014; Ochsner
& Gross, 2014). Furthermore, emotional regulation is an
umbrella term that can refer to any number of processes
but generally is used to indicate shaping one’s emotion
(Gross, 2014). In the laboratory, investigation of
emotional regulation requires systematic and focused
studies for teasing apart the various underlying neural
mechanism. Although the literature is replete with papers
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on emotional regulation, only a few of the papers report
using procedures that require voluntary emotional
responses (Fitzgerald et al., 2016; Ochsner & Gross,
2005; Urry et al., 2006). In these studies, subjects are
instructed to cognitively change their emotions by mod-
ifying their thoughts. By doing so, subjects attempt to vol-
untarily perform a cognitive reappraisal of the situation.
Although, most frequently, subjects are asked to decrease
negative emotions, cognitive reappraisal can be used to
increase or decrease both negative and positive emotions
(Ochsner et al., 2004). Previous studies have shown that
the medial (including the ventromedial PFC) and dorsal
prefrontal cortex (including the ventral and lateral
regions), and cingulate gyrus are involved in voluntarily
reducing emotions (Ochsner & Gross, 2005; Phan et al.,
2005; Urry et al., 2006).
An important and relevant emotional regulation
process involved in healthy functioning is the
suppression of negative emotions, or the attenuation
of the positive emotions, to mitigate emotions elicited
by contextual cues associated with relevant psychologi-
cally traumatic events. As such, cognitive and behavioral
therapies are aimed at improving one’s ability to
regulate emotions in response to trauma-related cues.
There have been efforts to understand the underpinning
neural functions of compromised emotional regulation
in the laboratory (Cisler et al., 2016; Johnstone, van
Reekum, Urry, Kalin, & Davidson, 2007; Urry et al.,
2006; van der Horn, Liemburg, Aleman, et al., 2016).
However, many studies only focus on populations
suffering from mood and stressor/trauma-related
disorders (e.g., depression, PTSD), fail to use an
appropriate control group, or do not use tasks that
require voluntary effort to regulate emotions. For
military service members, contextual cues can elicit
altered emotional responses (e.g., Goodman, Katz, &
Dretsch, 2016). Most efforts to explore emotional regu-
lation in military populations fail to use salient and
validated stimuli. Furthermore, many service members
experience psychological trauma, which contributes to
the high levels of comorbidity. During combat, being
exposed to life-threatening events such as exposure to
blast from explosive devices, which results in mTBI,
can be psychologically more traumatic than sustaining
an injury from a noncombat event (e.g., sporting event,
slipping in the shower). Because PTSD is linked to
emotional dysregulation, and there is a high comorbid-
ity of PTSD in service members with mTBI, a minimal
amount is known concerning the neural physiology
underlying mTBI in relation to emotional regulation.
Overall, emotional regulation following mTBI in mili-
tary populations is understudied in terms of using
objective measures for emotion research.
The current study was aimed at exploring if combat-
related mTBI is associated with emotional dysregulation
when controlling for PTSD symptoms. This aim was
accomplished by comparing neural activation in prior
deployed Army soldiers with and without mTBI during
an emotional regulation task adapted for functional
magnetic resonance imaging (fMRI; Urry et al., 2006),
and modified to include military-relevant, visual combat
stimuli. The findings have important implications to the
understanding of the underlying neurocircuitry
associated with emotional regulation in both healthy and
combat-injured military service members and veterans.
Method
Recruitment
Active-duty male and female soldiers between the ages
of 18 and 50 years were recruited from Fort Rucker,
AL and Fort Benning, GA to voluntarily participate in
the current study. The participant sample (N ¼ 72)
was mostly male (90.3%) with a mean age of 31.5 years
old (SD ¼ 6.0). Ethno-racially, the sample was mostly
Caucasian (65.3%) followed by African-American
(18.1%), Hispanic/Latino (12.5%), Asian (2.8%), and
Native American (1.4%). The majority of participants
were right-handed (91.7%). Recruitment consisted of
advertisements distributed and posted at local facilities
including the TBI Clinic. Soldiers receiving a
comprehensive evaluation and/or treatment at the
instillation TBI clinic were referred to the study by the
treating clinician and provided contact information to
voluntarily pursue participation. Soldiers provided
written informed consent prior to their enrollment in
the study. Data were collected at the Auburn University
MRI Research Center.
The study was carried out in accordance with the
latest version of the Declaration of Helsinki and the

protocol and procedures were approved by Auburn
University’s Institutional Review Board (IRB) and the
IRB at Headquarters U.S. Army Medical Research and
Materiel Command (HQ USAMRMC IRB).
Participants
Exclusion criteria were as follows: (a) pre-existing, non-
TBI neurologic disorder, psychotic disorder (e.g.,
schizophrenia); (b) bipolar disorder; (c) history of mod-
erate-to-severe TBI; and (d) contraindications to MRI.
All participants were screened for MRI contraindica-
tions prior to recruitment and again the same day of
data collection. All participants were required to have
a history of deployment(s) to a combat environment.
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Eligibility for the mTBI group included: (a) referred
by a neuropsychologist from the military TBI Clinic;
(b) a documented combat-related mTBI that occurred
within the last five years; and (c) presenting symptoms
associated with a history of medically documented
mTBI(s). Controls were healthy active-duty soldiers
with no medical history of mTBI in the last five years
and no history of mild-to-moderate TBI. Soldiers’
electronic medical records were screened by the study
physician to ensure they met the eligibility criteria.
Emotional regulation task
Participants performed an emotional regulation task
modeled after the one implemented by Urry et al.
(2006). Participants were told that they would see an
Figure 1. A trial example of emotional regulation task for the maintain condition. Participants were instructed to maintain, enhance,
or suppress their emotional response to MAPS images that are military specific. After the regulation period ended participants
indicated how well they regulated their emotion using a button box.
APPLIED NEUROPSYCHOLOGY: ADULT 3
image on the screen in front of them, they would look
at it, and then they would receive one of three instruc-
tions and regulate their emotions accordingly. If they
saw the word “ENHANCE,” they were told to attempt
to amplify the intensity of their negative feelings toward
the picture. They could do so by imagining themselves
or a loved one in the same situation or by imagining
a more extreme outcome than the one presented. If they
saw the word “SUPPRESS,” they were told to reduce the
intensity of their negative feelings toward the picture.
They could do so by imagining the situation as fake
or unreal, or by imaging the presented situation had
an outcome better than the one within the context of
the picture. If they saw the word “MAINTAIN,” they
were instructed to continue attending to the picture
without positively or negatively changing their feelings.
After regulating their emotions according to the
instruction, participants were then asked to report
how successful they were in regulating their emotions.
Using an MR-compatible 4-button box (Current
Design, Philadelphia) response device, participants
responded by indicating whether they were “Not suc-
cessful,” “Somewhat successful,” or “Very successful.”
If participants had no emotion to regulate, they were
asked to choose a “No Emotion” option. After the
self-report period ended, an inter-trial interval (ITI)
with a fixation cue followed and the next trial began
(See Figure 1 for a representative trial). Each trial lasted
17 s, with the fixation cue being presented for 1 s, the
view instruction (where participants passively viewed
the stimulus) lasting between 3–7 s, the regulation
 4 M. N. DRETSCH ET AL.
instruction lasting between 5–8 s, and a 5 s time period
to self-report their regulation success. The duration of
the view and regulation instructions were counterba-
lanced to ensure that all trials were 17 s in duration.
An event-related design was used to present viewing
and regulation instructions while participants viewed
images during blood oxygen level-dependent (BOLD)
fMRI acquisition. There were 5 blocks of the emotional
regulation task. The first block was a practice block to
familiarize participants with the task and was conducted
outside of the scanner with 24 noncombat images
selected from the International Affective Picture System
(IAPS; Lang, Bradley, & Cuthbert, 2008). While
instructions were provided within the task, the instruc-
tions were also presented to the participant verbally by
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the researcher before the practice block began. The
remaining 4 blocks took place within the MRI scanner
with the images from the Military Affective Picture
System (details reported below; Goodman et al., 2016).
Once in the scanner, the instructions were presented
again before the first block. Each block contained
24-trials, with 6 repetitions of 4 trials: suppress
negative images, enhance negative images, maintain
negative images, and maintain neutral images.
The negative MAPS images were supposed to arouse a
negative emotion in the subject, while the neutral
MAPS images were supposed to not alter the preexisting
emotional state of the subject. These trials were
pseudorandomized so that no more than three trials
of the same regulation instruction were shown
consecutively.
Stimulus materials
All images were comprised of color photographs, with
approximate resolutions of 1024 � 768 or 768 � 1024,
for landscape and portrait orientations, respectively.
These images were drawn from the MAPS (Goodman
et al., 2016) which contain military relevant scenes
depicting emotional content ranging from both
unpleasant to pleasant and calm to arousing. The MAPS
contains 240 normed images based on healthy, noncom-
bat exposed military using the Self-Assessment Manikin
(SAM) similar to that of the IAPS (Lang et al., 2008). In
the current study, MAPS images were selected by the
experimenters based on previously normed ratings
(ranging from 1, most unpleasant, to 9, most pleasant
and 1, least arousing, to 9, most arousing) in order to
generate image subcategories of negative and neutral
emotional scenes. Seventy-two negative MAPS images
were selected by the experimenters on the basis of
content normatively rated as relatively unpleasant
(M ¼ 3.36, 95% CI [3.36, 3.94]) and arousing (M ¼ 4.83,
95% CI [4.62, 5.00]). Twenty-four neutral MAPS images
were selected on the basis of content normatively rated
as neither pleasant nor unpleasant (M ¼ 5.58, 95%
CI [4.94, 6.21]) with low arousal (M ¼ 2.63, 95%
CI [2.19, 3.08]). Independent samples t-tests, corrected
for unequal variances when necessary, confirmed that
the negative images were less pleasant, t(38.46) ¼ 8.00,
p < .05, and more arousing, t(73) ¼ 8.97, p < .05, than
the neutral images. Image presentation orders were
pseudorandomized in blocks of 4 image presentations,
with the constraint that each block contained 1 neutral
image. All experimental events and stimulus presenta-
tions were controlled and recorded using E-Prime 2.0
software (Psychology Software Tools) on a standard
PC. All images and instructions were presented using
a rear-bore projection screen and projector (Avotec
Silent Vision).
Procedures
Upon arrival at the Auburn University MRI Research
Center for their scheduled testing appointment,
participants were re-screened for eligibility and
re-consented to ensure full comprehension of the
study’s procedures. Participants completed a battery of
computerized neurocognitive tests and questionnaires
assessing demographics, medical history, and psycho-
logical health. After completion, participants were then
escorted to the MRI suite for the imaging portion of the
study. After completion of the study, participants
received monetary compensation for their time.
Psychological health and neurocognitive
measures
A battery of psychological health and neurocognitive
measures was administered to participants prior to their
MRI scan. The battery consisted of the Brief Traumatic
Brain Injury Screen (Schwab et al., 2006), PTSD
Checklist-5 (PCL; Blevins, Weathers, Davis, Witte, &
Domino, 2015), Neurobehavioral Symptom Inventory
(Cicerone, 1995), Life Events Checklist (Gray, Litz,
Hsu, & Lombardo, 2004), Combat Exposure Scale
(Guyker et al., 2013), Childhood Environment (King,
King, & Vogt, 2003), Zung Depression Scale (Zung,
Richards, & Short, 1965), Zung Anxiety Scale (Zung,
1971), Alcohol Use Dependency Identification Test
(Saunders, Aasland, Babor, De la Fuente, & Grant,
1993), Epworth Sleepiness Scale (Johns, 1991), and the
Automated Neuropsychological Assessment Metrics
(ANAM) Version 4 (Appendix 1).
In addition, we also tested effort to improve the
validity of our assessment data. To this end, we

administered the Test of Memory Malingering (Tom-
baugh, 2003), which consists of two learning trials and
a retention trial that uses pictures of common, everyday
objects (e.g., chair, pencil). A cut-off score (<45 correct)
was used to determine eligibility for participation in the
study. All participants passed the first trial.
Statistical analysis for self-report and
neurocognitive measures
Nominal and ordinal data were analyzed using Chi
squared (v2) and Kendall’s tau-b (Tb). Student’s t-tests
were used to explore group mean differences on
self-report and neurocognitive measures (Benjamini-
Hochberg adjusted to control for false discovery rate).
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For the ratings of perceived success at regulating
emotion, two-way repeated-measures analysis of
variance (ANOVA) of Group (mTBI, Control) x
Instruction (enhance, maintain, suppress) and Group
x Stimulus Type (negative, neutral) were used to analyze
the data.
Imaging acquisition
Soldiers were scanned in a 3TVerio scanner (Siemens
Healthcare, Erlangen, Germany) using T2* weighted
multiband echo-planar imaging (EPI) sequence with
TR ¼ 600 ms, TE ¼ 30 ms, FA ¼ 55˚, multiband
factor ¼ 2, voxel size ¼ 3.5 � 3.5 � 5 mm3, 680 volumes
per run and 4 runs per subject. Total acquisition time
was approximately 6 min and 48 s per scan and 27 min
and 12 s overall (for the ERT runs). A 32-channel head
coil (Siemens Healthcare, Erlangen, Germany) outfitted
with a mirror was used. Stimuli were presented using
an Avotec Silent Vision LCD projection system.
Anatomical data was obtained using the magnetization-
prepared rapid gradient echo (MPRAGE) sequence using
the following parameters: TR ¼ 1900 ms, TE ¼ 2.5 ms,
FA ¼ 9˚ and voxel size ¼ 1 � 1 � 1 mm3
Functional data preprocessing
Functional data were preprocessed and analyzed using
FMRIB’s Software Library fMRI Expert Analysis Tool
(FSL FEAT, Smith et al., 2004). Specifically, for prepro-
cessing, data were brain extracted, slice-time corrected,
smoothed (5 mm FWHM Gaussian kernel), high-pass
filtered, motion corrected using FSL’s MCFLIRT
(Jenkinson, Bannister, Brady, & Smith, 2002), realigned,
and registered to each individual’s high-resolution ana-
tomical data, and normalized to Montreal Neurological
Institute (MNI) standard space using FLIRT (Jenkinson
et al., 2002; Jenkinson & Smith, 2001). Data were also
APPLIED NEUROPSYCHOLOGY: ADULT 5
subjected to multiple regression using a prewhitening
technique to account for intrinsic autocorrelations of
the blood-oxygen-level-dependent (BOLD) signal.
Functional data analysis
First-level contrasts were created to examine the effect
of emotion regulation on participants’ neural activity.
During the emotional regulation task, we considered
only activity during the “regulation” phase of the trial
(cf. Figure 1). Parameter estimates were generated for
each voxel independently for the various regulation
conditions, and contrasts between the estimates were
used to create the statistical images (i.e., to determine
the effects of “suppression” and “enhancement,”
estimates from when participants were given the
“suppress” or “enhance” instruction during negative
imagery were contrasted against estimates during the
“maintain” condition at each voxel independently). In
order to determine the effects of negative valenced
images, we compared parameter estimates from when
participants were given the “maintain” instruction for
neutral imagery to the same instruction for negative
imagery. After first-level analyses were completed,
second-level analyses were conducted to combine each
participant’s runs together. The resultant statistical
maps were then subjected to group level contrasts to
compare mTBI and Control groups using mixed effects
modeling, controlling for PTSD symptoms by using
PCL scores as a covariate. Specifically, PCL scores were
mean centered across all subjects allowing for resulting
inferences to be adjusted for any PCL score differences
between groups. We also examined the main effect of
PCL score. Group maps were thresholded based on
the magnitude (z ≥ 2.3) and extent (cluster p < 0.05)
of activation. This second-level analysis was implemen-
ted to assess differential neural activity during emotion
regulation conditions across groups. Resultant MNI
coordinates were converted to Talairach space using
Lancaster et al.’s (2007) icbm2tal transform, and regions
were identified using the Talairach Client (http://www.
talairach.org/manual.html).
Results
Group differences are shown in Table 1. There were
significant differences between the mTBI (n ¼ 37) and
Control (n ¼ 35) groups in the distribution of females,
v2 ¼ 8.20, p ¼ .004. There were no significant differ-
ences between the groups in terms age or rank, p > .05.
There were significant group differences with the Con-
trol group being slightly more educated, t(67) ¼ 2.66,
p ¼ .010, than the mTBI group. As expected, the
 6 M. N. DRETSCH ET AL.

Table 1. Group characteristics. Neurofunctional differences in emotion

Variable Controls (n ¼ 35) mTBI (n ¼ 37) regulation
Age, M(SD) 30.9 (6.8) 32.1 (5.2)
Gender, male 80.00% 100.00% After controlling for PTSD symptoms, the only signifi-
Education HS graduate 11.80% 26.50% cant group differences were observed in the “enhance”
Some college 26.40% 41.20%
College graduate 61.80% 32.40% condition with the mTBI group showing hyperactiva-
Rank/grade Enlisted 20 (57%) 32 (86%) tion in primarily compared to the Control group
Warrant 8 (23%) 0 (0%)
Officer 7 (20%) 5 (14%) (Figure 2). As shown in Table 4, the mTBI group
Combat exposure, M(SD) 7.8 (9.6) 29.1 (8.4) showed significantly greater BOLD signal compared to
Note. HS ¼ High School. controls in the left precentral gyrus, bilaterally in the
postcentral gyrus, right inferior parietal lobe (IPL), left
participants in the mTBI group had higher combat insula, and left superior temporal gyrus (STG). There
exposure scores, t(65) ¼ 9.84, p < .001, and a greater were no significant group differences in BOLD acti-
number of lifetime mTBIs, t(43) ¼ 3.08, p < .001, than vation during either the maintain or suppress
the Control group. As shown in Table 2, there were sig- conditions.
As illustrated in Figure 3, in the enhance condition,
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nificant differences between the groups with the mTBI

group reporting higher scores of alcohol use, postcon-
cussive symptoms, daytime sleepiness, sleep quality,
traumatic life events, PTSD symptoms, and symptoms
of anxiety and depression, p < .05. The effect sizes for
these measures ranged from medium to very large
(d ¼ 0.65–3.22). There were no significant differences
in negative childhood experiences, p > .05. Shown in
Table 3, only on the simple reaction time subtest
of the ANAM did the mTBI group have significantly
lower scores than controls (p < .05; d ¼ 0.53, medium
effect size).
Emotion regulation ratings
The results indicated there were no significant
differences in mean ratings of self-reported success
between the mTBI and Control groups across regulation
conditions with negative stimuli (enhance: M ¼ 2.80, CI
[2.63, 2.96]; maintain: M ¼ 2.73, CI [2.54, 2.91];
suppress: M ¼ 2.66, CI [2.51, 2.83]), all F’s < 1.73,
ps > .18. This lack of significant findings replicates
those reported in Urry et al., 2006. The results revealed
a significant main effect of stimulus type, F(1, 70) ¼
18.28, p < .05, ηp2 ¼ 0.21, suggesting that, overall,
participants had higher success ratings for regulating
negative stimuli (M ¼ 2.73, CI [2.58, 2.88]).
there was a main effect of PTSD symptoms on neural
activity on primarily the right frontal regions, but also
left frontal regions, and less of an overall impact on
limbic regions (Table 5).
Discussion
The findings suggest that symptomatic soldiers with
combat-related mTBI have a quantifiably different
neural pattern associated with voluntary regulation of
emotions than deployment exposed controls. Using a
task consisting of military relevant images, only when
instructed to enhance (i.e., make the negative feelings
toward images more extreme) did the mTBI group show
significant differences in neural activation, namely
hyperactivation, compared to controls. These regions
included areas associated with cognitive-emotional
processes such as the pre- and postcentral gyri, inferior
parietal lobe (IPL), insula, and superior temporal
gyrus (STG).
As expected, the mTBI group reported greater
symptoms on a number of psychological health mea-
sures. As such, one inherent limitation of doing mTBI
research in military personnel is the high comorbidity
with other psychological conditions such as PTSD
(Dretsch, Williams, et al., 2016; Hoge et al., 2008; Jaffee,

Table 2. Mean (standard deviation) differences, effect sizes (d), and confidence intervals (CI) between Control group and mTBI group
on psychological health measures.
Group PCL NSI AUDIT LEC ESS ZAS ZDS CE
Control
M(SD) 30.06 (12.86) 9.35 (9.39) 4.74 (4.05) 37.89 (14.63) 9.21 (3.67) 30.11 (8.26) 32.26 (9.64) 54.15 (12.68)
mTBI
M(SD) 72.89 (13.74) 44.97 (15.17) 8.63 (7.96) 22.08 (10.47) 13.43 (5.43) 50.86 (9.12) 53.06 (9.53) 52.26 (12.54)
d 3.22* 2.89* 0.65* 1.26* 0.93* 2.39* 2.17* 0.15
95% CI 49.2, 29.5 9.8, 21.8 6.9, 0.8 9.8, 21.8 6.4, 2.0 24.9, 16.6 25.4, 16.2 4.2, 7.9
Note. PCL ¼ PTSD Checklist-5; NSI ¼ Neurobehavioral Symptom Inventory; AUDIT ¼ Alcohol Use and Dependency Identification Test; LEC ¼ Life Events
Checklist; ESS ¼ Epworth Sleepiness Scale; ZAS ¼ Zung Anxiety Scale; ZDS ¼ Zung Depression Scale; CE ¼ Childhood Environment.
*p � .05 (Benjamini-Hochberg adjusted).
 APPLIED NEUROPSYCHOLOGY: ADULT 7

Table 3. Mean (standard deviation) differences, effect sizes (d), and confidence intervals (CI) between Control group and mTBI group
on standardized throughput scores on ANAM subtests.
ANAM Subtest
Group SRT SRT2 PRT CDS CDD MTS MTH
Control
M(SD) 103.86 (14.16) 104.32 (14.58) 104.98 (15.71) 105.45 (15.94) 104.37 (15.34) 102.16 (16.91) 101.35 (15.97)
mTBI
M(SD) 95.71 (16.73) 96.00 (16.19) 97.11 (13.95) 94.94 (13.66) 96.87 (14.92) 96.08 (15.09) 98.65 (15.82)
d 0.53* 0.54 0.53 0.71 0.50 0.38 0.17
95% CI 0.88, 15.43 1.08, 15.55 0.89, 14.84 0.39, 14.61 3.54, 17.47 1.44, 13.63 4.78, 10.17
Note. Higher standardized scores ¼ better performance. SRT ¼ Simple Reaction Time; SRT2 ¼ Simple Reaction Time-Delayed; PRT ¼ Procedural Reaction Time;
CDS ¼ Coded Substitution Test; CDD ¼ Coded Substitution-Delayed; MTS ¼ Matching to Sample; MTH ¼ Mathematical Processing.
*p � .05 (Benjamini-Hochberg adjusted).

Stokes, & Leal, 2007; Kontos et al., 2013; Walker, stimuli used in the task are negatively valenced (e.g.,
Franke, McDonald, Sima, & Keyser-Marcus, 2015). This perceived as threatening), individuals with PTSD show
is most likely due to qualitative differences in events what is described as attentional bias (Sipos, Bar‐Haim,
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between combat-related mTBI in military personnel
versus noncombat mTBI in civilians.
There is evidence suggesting mTBI is associated with
cognitive impairments (Spira, Lathan, Bleiberg, & Tsao,
2014), but this is not always the case (Dretsch,
Silverberg, et al., 2015). More consistently, cognitive
impairments have been associated with PTSD (Dretsch,
Thiel, Athy, Irvin, et al., 2012). However, when the
Figure 2. Group differences during enhancement (Enhance -
Negative Maintain) for mTBI > Controls. Warmer colors indicate
higher z-statistics.
Abend, Adler & Bliese, 2014). In the current study,
our mTBI group with elevated PTSD symptoms showed
a mild decrement in attention as assessed via simple
reaction time. Since this task consists of neutral stimuli,
we cannot rule out an attentional bias toward the
negatively valenced stimuli presented in the emotional
regulation task.
Prior evidence indicates soldiers with PTSD are
hypersensitive to aversive stimuli (Dretsch et al.,
2012), which appears to be linked with differences in
their neurocircuitry associated with hypersensitivity to
threat (Dretsch, Wood, et al., 2016). Considering this
evidence, it was necessary to control for PTSD symptom
severity when comparing groups during the specific
conditions of the emotion regulation task.
When controlling for PTSD symptoms, the mTBI
group had significantly greater activation in neural
regions during the enhance condition that might reflect
compromised cognitive-emotional processing; pre- and
postcentral gyri, inferior parietal lobe (IPL), insula, and
superior temporal gyrus (STG). The precentral gyrus
forms part of the supplementary motor area (pre-
SMA); with connections to the PFC, and functionally
linked with language and memory tasks (Johansen-Berg
et al., 2004; Kohn et al., 2014). The precentral gyrus has
been liked with employing self-focused or situation-
focused reappraisal strategies to increase or decrease
emotion (Ochsner et al., 2004) and viewing positive
valenced images (Seo et al., 2013). The IPL has been
implicated in the interpretation of sensory and
emotional information (Nomi et al., 2008; Pessoa,
Kastner, & Ungerleider, 2002). The postcentral gyrus
is the principle somatic sensory region, which shows
increased activation while enhancing emotions associa-
ted with negative valenced images (Ochsner et al., 2004).
The STG has been linked with facial processing and
social cognition (Adolphs, 2001; Haxby, Hoffman, &
Gobbini, 2000). Lastly, the insula has been implicated
 8 M. N. DRETSCH ET AL.

Table 4. Comparison of neural activation between mTBI versus Controls.

Enhance > Negative Maintain
mTBI > Controls (controlling for PCL scores)
z-score x y z Lobe Region Brodmann Area
3.61 45.67 9.53 37.65 Frontal Left Precentral Gyrus 6
3.45 54.12 8.66 10.51 Left Precentral Gyrus 43
3.64 53.29 20.01 38.73 Parietal Left Postcentral Gyrus 3
3.74 35.63 31.27 39.45 Right Inferior Parietal Lobule 40
3.73 37.52 31.35 40.36 Right Inferior Parietal Lobule 40
3.73 51.75 21.10 42.02 Right Postcentral Gyrus 2
3.65 29.93 33.47 44.70 Right Postcentral Gyrus 3
3.65 33.72 33.56 45.62 Right Postcentral Gyrus 3
3.71 37.06 1.40 13.80 Sub-lobar Left Insula 13
3.75 53.16 8.44 6.91 Temporal Left Superior Temporal Gyrus 22
3.48 45.62 19.77 4.41 Left Superior Temporal Gyrus 22
Note. Reported coordinates are in Talairach space.

in emotional-awareness and interoceptive awareness with increased BOLD signal in both prefrontal and lim-
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(Garfinkel & Critchley, 2013; Gu, Hof, Friston, &
Fan, 2013).
It is unlikely the results of the current study were
explained by PTSD symptoms in the mTBI group since
we controlled for this in the analysis. In support of this,
there was a main effect of PTSD symptoms on neural
activation during the enhance condition. The findings
suggest that elevated PTSD symptoms were associated
Figure 3. Main Effect of PTSD symptoms (PCL scores) on
enhancement (Enhance - Negative Maintain) for mTBI >
Controls. Warmer colors indicate higher z-statistics.
bic regions. These regions included areas commonly
associated with regulation of emotion, especially the
medial prefrontal cortex and cingulate gyrus (Ochsner
& Gross, 2005; Urry et al., 2006), and have been
implicated in regulation emotions in both civilian and
military populations with PTSD (Dretsch, Wood,
et al., 2016; Greco & Liberzon, 2016).
Alternatively, other psychological health symptoms
could account for the significant neural hyperactivation
during the enhance condition, especially since
depression scores were greater than those reported by
controls. We did not control for depression due to
issues of multicollinearity and the potential of over-
fitting. However, prior findings using a similar task
have linked depression with greater activation in right
prefrontal cortex, but in the suppress condition only
(Johnstone et al., 2007). In contrast, our study
showed significant hyperactivation of multiple ROIs
that have been implicated in both cognitive and
affective processes, but only in the enhance condition,
not the suppression condition. As such, multiple
differences in clinical populations recruited by
Johnstone et al. and our study are likely to underlie
differences in findings.
Based on the functional imaging findings, an
attentional bias toward negatively valenced stimuli in
the mTBI group may be a cogent explanation. However,
since these findings were not observed during the
maintain condition, it is likely that hyperactivation in
the enhance condition is a result of a susceptibility to
heightened responses to relevant stimuli when
prompted. For example, the contextual images from
the MAPS may have elicited greater emotions associated
with prior combat experiences that resulted in the part-
icipants’ injuries. Although we controlled for PTSD
symptoms, this hyperactivation could be driven by
greater propensity for increased neural activity when
prompted (explicitly) or potentially implicitly (i.e., when
 APPLIED NEUROPSYCHOLOGY: ADULT 9

Table 5. Main effect of PTSD symptoms on neural activation.

Enhance > Negative Maintain
Main Effect of PCL Score
z-score x y z Lobe Region Brodmann Area
4.37 18.99 30.09 25.01 Frontal Left Medial Frontal Gyrus 9
3.11 25.61 32.10 24.19 Left Middle Frontal Gyrus 9
3.64 16.00 32.76 38.06 Right Medial Frontal Gyrus 8
3.53 14.14 36.86 33.80 Right Medial Frontal Gyrus 9
3.51 17.96 41.14 25.95 Right Medial Frontal Gyrus 9
3.44 11.31 38.84 33.00 Right Medial Frontal Gyrus 9
3.34 19.80 29.46 29.73 Right Medial Frontal Gyrus 9
3.84 16.97 38.50 37.54 Right Superior Frontal Gyrus 9
3.39 19.04 19.43 27.93 Limbic Left Cingulate Gyrus 32
3.33 19.03 22.27 28.12 Left Cingulate Gyrus 32
Note. Reported coordinates are in Talairach space.

left to one’s own devices: counterfactual thinking). them more likely to sustain an mTBI (Dretsch, Silver-
Alternatively, or in combination, the results might be berg, et al., 2016; Dretsch, Williams, et al., 2016;
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explained by dysregulation of the neurocircuitry due
to injury pathophysiology (e.g., potentially a result of
frontal and anterior neuronal contusion, axonal injury,
and/or from secondary biochemical and metabolic
changes; Dretsch, 2010; Eierud et al., 2014; Little et al.,
2014). Interestingly, there were no significant differ-
ences in self-reported success in enhancing emotional
responses to support perceived difficulty on behalf of
the participants. Regardless of the precise mechanistic
underpinning reason, to the best of our knowledge, this
is a first to illustrate a relationship between increased
emotional load and the underpinning neurophysiologic
correlates in a military mTBI population while control-
ling for PTSD symptoms.
Panenka et al., 2017). Furthermore, some individuals
may be less resilient to the effects of mTBI and combat
and, therefore, develop persistent present postconcus-
sive symptoms and continue to seek treatment. As such,
it is feasible that patients recruited and enrolled in the
mTBI group may have had a similar abnormal pattern
of neural activation prior to their injury(s). Finally,
given that some of the MAPS images contain faces of
both civilians and soldiers, it might be valuable to
explore whether differences in neural activation was
associated with a general response (vigilance) to combat
images or moderated by specific image content (e.g.,
faces versus no faces).

Limitations
In the current study, we controlled for PTSD symptoms
in our imaging analysis. Given that the mTBI group also
had significantly greater psychological health symptoms
including anxiety and depression, and potential
for greater aversive medication interactions from
polypharmacy use, it cannot be ruled out that the
findings are partially explained by factors other than
mTBI pathophysiology alone. Future efforts should
attempt to address the impact of these factors on
emotional regulation. An alternative explanation for
the findings could be due to unintentional selection bias
during the recruitment phase rather than the product of
injury/trauma-related neurobiological changes. In this
scenario, individuals with mTBI would have been
vulnerable to persistent complaints based on their pre-
morbid ability to emotionally regulate. Hence, the find-
ing of abnormal neural activation associated with task
performance could reflect a specific phenotype or inter-
mediate phenotype of vulnerability. Evidence suggests
some individuals have a genetic predisposition making
Conclusion
The findings in the current study revealed that in
soldiers with a history of deployment, there is a different
pattern of neural activation in those with mTBI
compared to those without when instructed to volun-
tarily enhance emotional responses to combat-related
visual stimuli. These differences were not explained by
elevated PTSD symptoms in the mTBI group as this
was controlled for in our analysis. Significant group
differences were not observed during either the main-
tain or suppress conditions. Hyperactivation of neural
regions in the mTBI group during the enhance
condition may reflect underlying vigilance towards
negative contextual stimuli and/or poor strategy that
might result in poor allocation of resources to regulate
emotions. It is likely that this abnormal pattern
contributes to the development and maintenance of per-
sistent postconcussive symptoms following mTBI. How-
ever, whether this pattern is associated with injury-
related pathophysiology, comorbid psychological health
conditions, an intermediate phenotype, or a
combination of these factors, remains unclear.
 10 M. N. DRETSCH ET AL.
Acknowledgments
The authors acknowledge the assistance of numerous indivi-
duals from the U.S. Army Aeromedical Research Laboratory
and Auburn University for their critical role and diligent
effort during the data collection phase.
Disclaimer
The views expressed in this article are those of the authors and
do not reflect the official policy of the Department of Defense
or U.S. Government.
Funding
This project was funded by the U.S. Army Medical Research
Downloaded by [Australian Catholic University] at 04:54 23 September 2017
and Materiel Command (USAMRMC), Military Operational
Medicine Research Program, and was supported in part by
an appointment by the Internship/Research Participation Pro-
gram, Oak Ridge Institute for Science and Education (ORISE),
through an agreement between the U.S. Department of
Energy and the USAMRMC.
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Appendix A. psychological health measures
a) PTSD Checklist-5 (PCL-5; Blevins et al., 2015). The
PCL-5 is a 20-item self-report measure that assesses
the 20 Diagnostic and Statistical Manual of Mental
Disorders, Fifth Edition (DSM-5) symptoms of
PTSD. The PCL-5 has a variety of purposes,
including screening individuals for PTSD, making
provisional PTSD diagnoses, and monitoring symp-
tom change during and after treatment, Items are
rated using a 5-point Likert scale; 0 ¼ “Not at all”
to 4 ¼ “Extremely.” A total symptom severity score
(range 0–80) can be obtained by summing the
scores for each of the 20 items with a cut score of
38 for a provisional diagnosis of PTSD.
b) Life Events Checklist (LEC; Gray, Litz, Hsu, &
Lombardo, 2004). The LEC is a brief, 17-item,
self-report measure designed to screen for poten-
tially traumatic events in a respondent’s lifetime.
The LEC assesses exposure to 16 events known to
potentially result in PTSD or distress and includes
one item assessing any other extraordinarily stressful
event not captured in the first 16 items. For each
item, the respondent checks whether the event (a)
happened to them personally, (b) they witnessed
the event, (c) they learned about the event, (d) they
are not sure if the item applies to them, and (e) the
item does not apply to them. The instrument has
modest retest reliability (0.82).
c) Combat Exposure Scale (CES; Guyker et al., 2013).
The CES is a 7-item self-report measure that assesses
wartime stressors experienced by combatants. Items
are rated on a 5-point frequency, 5-point duration,
4-point frequency, or 4-point degree of loss scale.
d) Childhood Environment (CE; King, King, & Vogt,
2003). The Deployment Risk and Resilience Inven-
tory (DRRI) is a set of 13 subscales that evaluate a
number of risk and recovery factors during different
stages of deployment that might affect an indivi-
dual’s development of stress-related illness. We
included the CE to explore the effects of positive
and negative childhood experiences that might
impact the development of emotional regulation.
e) Brief Traumatic Brain Injury Screen (BTBIS; Schwab
et al., 2006). This 3-item assessment is used by the
Army for identifying soldiers that may have

sustained a mild TBI. Subjects identify the mech-
anism (e.g., fragment, vehicular, blast), symptoms
immediately after the injury, and current symptoms
believed to be associated with an injury. A mTBI
positive score required both the endorsement of an
injury-related event, and at a minimum, an altered
state of consciousness (e.g., being dazed, confused,
or seeing stars; posttraumatic amnesia; loss of
consciousness <20 minutes).
f) Neurobehavioral Symptom Inventory (NSI; Cicerone,
1995). The NSI is a 22-item measure designed to
evaluate self-reported postconcussion symptoms
(e.g., headache, balance problems, nausea, fatigue,
sensitivity to noise, irritability, sadness, nervousness,
difficulty concentrating, difficulty remembering, visual
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problems) on a scale from 0 to 4. The scale yields a
total score ranging from 0–88.
g) Zung Depression Scale (ZDS; Zung, 1971a). The ZDS
is a 20-item scale measuring self- reported symptoms
of depression. The ZDS produces scores ranging
from 20 through 80; 20–44 for normal range, 45–59
for mildly depressed, 60–69 for moderately
depressed, and 70 and above for severely depressed.
h) Zung Anxiety Scale (ZAS; Zung, 1971b). This ZAS is
a 20-item, self-report anxiety rating scale. The ZAS
has scores ranging from 20 through 80; 20–44 for
normal range, 45–59 for mild to moderate anxiety,
60–74 for marked to severe anxiety, and 75–80 for
extreme anxiety.
APPLIED NEUROPSYCHOLOGY: ADULT 13
i) Alcohol Use Dependency Identification Test
(AUDIT; Saunders, Aasland, Babor, De la Fuente,
& Grant, 1993). The 10-item instrument is used to
assess alcohol use. A score of 8 or more in men,
and 7 or more in women, indicates likelihood of
hazardous or harmful alcohol use. A score of 20 or
more suggests potential alcohol dependence.
j) Epworth Sleepiness Scale (ESS; Johns, 1991). This
instrument asks the subject to rate his or her
probability of falling asleep on a scale of
increasing probability from 0 to 3 in eight different
situations.
k) Automated Neuropsychological Assessment Metrics
(ANAM) Version 4. The ANAM is a reliable auto-
mated, computerized neurocognitive assessment that
includes six subtests: Simple Reaction Time (SRT),
Procedural Reaction Time (PRT), Code Substitution
Learning (CSL), Matching-to-Sample (M2S), Math-
ematical Processing (MTH), Code Substitution
Delayed (CSD), and Simple Reaction Time Repeated
(SRT2). The ANAM records accuracy, speed, and
throughput (TP) performance for each subtest. TP
is a single outcome measure produced from percent-
age correct (accuracy) divided by mean reaction time
(speed). Therefore, TP scores represent the correct
number of responses per minute of available
response time; thus, higher values indicate better
performance. Standardized TP scores were used in
the analysis.