NeuroRehabilitation 37 (2015) 89–98 89

DOI:10.3233/NRE-151242
IOS Press

Examining cognitive emotion regulation

in frontal lobe patients: The mediating role
of response inhibition
Rosalux Falqueza,∗ , Ramona Dinu-Biringera,b , Malte Stopsacka , Elisabeth A. Arensa ,
Wolfgang Wickc and Sven Barnowa
a Institute of Psychology, Department of Clinical Psychology and Psychotherapy, University of Heidelberg, Germany
b Central Institute of Mental Health, Mannheim, Germany
c Neuro-oncology Department, University Hospital, Heidelberg, Germany

Abstract.
BACKGROUND: Previous investigations have demonstrated the relationship between inhibitory deficits and maladaptive emotion
regulation. Although several neuropsychological studies show that frontal lobe damage can lead to extreme inhibition impairments,
there have been no investigations regarding the influence of frontal lobe damage and related inhibition impairments on the use of
maladaptive strategies.
OBJECTIVE: The goal of the current study was to examine the impact of executive functions impairments due to frontal lobe
damage on cognitive emotion regulation.
METHODS: Fifteen patients with frontal lobe damage were compared to twenty-two healthy controls on their reported use of
maladaptive strategies. The effect of behavioral inhibition deficits among the frontal lobe damage group was examined.
RESULTS: Patients reflected a heightened use of maladaptive strategies compared to healthy controls, significantly mediated by
Go/NoGo task errors, which are an indicator for response inhibition deficits.
CONCLUSIONS: Results suggest that a heightened use of maladaptive strategies by patients relies to a strong extent on their
impaired impulse control, highlighting the complex interplay between executive functions and emotional regulation.

Keywords: Frontal lobe lesion, emotion regulation, response inhibition, maladaptive strategies

1. Introduction Nolen-Hoeksema, 2012a, 2012b). For example, we may

In order to adjust our emotions to certain desired
states or situations, we draw on several strategies
for emotion regulation (ER). The chosen strategies
should allow us to modify our emotions suitable to
changing intern or extern environments (Aldao &
∗ Address for correspondence: Rosalux Falquez, Institute of Psy-
chology, Department of Clinical Psychology and Psychotherapy,
University of Heidelberg, Hauptstrasse 47-51, 69117 Heidelberg,
Germany. Tel.: +49 6221 547748; Fax: +49 6221 547348; E-mail:
rosalux.falquez@psychologie.uni-heidelberg.de.
suppress negative emotions in an uncomfortable job sit-
uation due to the professional context. Later on, we may
either express our negative emotions by crying out loud,
or distract ourselves from negative feelings. To date,
there are several studies showing that ER strategies
are strongly associated with psychopathology, espe-
cially if these are rigidly used or implemented in an
inflexible way (Barnow, Aldinger, Ulrich, & Stopsack,
2013; Malooly, Genet, & Siemer, 2012). ER-strategies
like rumination, self-blame, catastrophizing or blam-
ing others may, for instance, narrow attentional focus

1053-8135/15/$35.00 © 2015 – IOS Press and the authors. All rights reserved
90 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients
to negative stimuli preventing an appropriate emotional
adjustment to the given context (Barnow, 2012; Garnef-
ski, Koopman, Kraaij, & ten Cate, 2009; Yoon, Maltby,
& Joormann, 2012; Zetsche, D’Avanzato, & Joormann,
2012).
Previous functional imaging studies examining the
neural correlates of ER have emphasized the role
of the frontal lobes (FL) on the down-regulation of
emotional responses (Banks, Eddy, Angstadt, Nathan,
& Phan, 2007; Buhle, et al., 2013; Goldin, Mcrae,
Ramel, & Gross, 2008a). Because of the reciprocal
connections with subcortical emotion systems such
as amygdala, the FL have a major role in emotional
processing and are in constant interplay with “bottom-
up” mechanisms (Wager, Davidson, Hughes, Lindquist,
& Ochsner, 2008). Similarly, studies of patients with
damage affecting the FL report impaired emotional
and social interactions (Bramham, Morris, Hornak,
Bullock, & Polkey, 2009), including inappropriate,
automatic behaviors (eg., emotional outburst, irritabil-
ity, etc; Rodriguez-Bailon, Trivino, & Lupianez, 2012).
Several neuropsychological studies have shown that the
FL are referred to be critical for the ability to moni-
tor and update relevant information about the current
context in order to inhibit prepotent thoughts or motor
responses (Badre, 2008; Dimitrov, Grafman, & Holl-
nagel, 1996; Garavan, Ross, Murphy, Roche, & Stein,
2002; Miyake, et al., 2000). Therefore, patients with
FL-damage often seem to ignore environmental cues,
so that they poorly adapt to new situations and are insen-
sitive to social feedback (Lezak, Howieson, Bigler, &
Tranel, 2012). These faculties allowing individuals to
draw mental or behavioral “shifts” according to con-
text are defined in the literature as executive functions
(EF), which describe a set of higher-order cognitive pro-
cesses (Demakis, 2004; Garavan et al., 2002; Hofmann,
Schmeichel, & Baddeley, 2012) including cognitive
inhibition, updating and switching abilities (Miyake,
et al., 2000), all mostly related to the integrity of the FL
(Allain, Etcharry-Bouyx, & Le Gall, 2001; Kimberg &
Farah, 1993; Tsuchida & Fellows, 2012).
It has been demonstrated that maladaptive emotion
regulation strategies are highly associated with inhibi-
tion deficits (Gotlib & Joormann, 2010; Joormann &
Gotlib, 2010a; Zetsche et al., 2012). For example rumi-
nation, i.e., thinking repetitively about negative events,
emotions or meanings, might rely on difficulties in
inhibiting negative thoughts. This maladaptive strategy
is strongly linked with sustained negative affect (Joor-
mann & D’Avanzato, 2010; Nolen-Hoeksema, 2000),
depression (Barnow et al., 2013; Cooney, Joormann,
Eugene, Dennis, & Gotlib, 2010) and stress-related car-
diovascular diseases (Verkuil, Brosschot, de Beurs, &
Thayer, 2009). Moreover, response inhibition deficits
are also an important aspect of several psychiatric dis-
orders such as borderline personality disorder (Arens,
et al., 2013; Lang, et al., 2012; Rentrop, et al., 2008),
obsessive compulsive disorder (Bannon, Gonsalvez,
Croft, & Boyce, 2002; Penades, et al., 2007; Ruchsow,
et al., 2007), substance use disorder (Morein-Zamir &
Robbins, 2014), and binge eating disorders (Svaldi,
Brand, & Tuschen-Caffier, 2010), which in turn are
characterized by the use of maladaptive ER strategies
(Aldao, Nolen-Hoeksema, & Schweizer, 2010).
To sum up, although there are consistent findings
about the association between executive inhibition and
the use of ER strategies, to our knowledge no study
has examined the effect of executive impairments due
to a lesion in the FL on cognitive ER. Thus, the
aim of this study was to extend previous findings by
examining the role of the FLs on maladaptive ER.
More specifically, we compared FL-damaged patients
with healthy controls (HC) in the use of adaptive and
maladaptive ER strategies and hypothesized that FL-
damaged patients use maladaptive ER strategies more
often than HC. Given that inhibition deficits play a
crucial role on emotional dysregulation, we tested if
the differences between FL-damaged patients and HC
can be explained by response inhibition impairments.
Other relevant cognitive deficits associated with FL-
damage, as for example memory recall (Wheeler, Stuss,
& Tulving, 1995) and cognitive flexibility (Cato, Delis,
Abildskov, & Bigler, 2004; Delis, Squire, Bihrle, &
Massman, 1992), were included as control variables. In
addition, given that depression has been strongly asso-
ciated with the use of maladaptive emotion regulation
strategies in the past (Aldao & Nolen-Hoeksema, 2010;
Barnow et al., 2013; Joormann & D’Avanzato, 2010;
Joormann & Gotlib, 2010b), the influence of depressive
symptomatology was also examined.
2. Material and methods
2.1. Participants
A total of seventeen right-handed adults with cor-
tex lesions primarily affecting the FL (16 brain
tumors, 1 cyst), were recruited either from the Neu-
rooncology Department of the University Hospital in
Heidelberg, through advertisements posted in news-
papers, or from support groups in the community.
 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients
The inclusion criterion was the presence of a lesion
involving well-defined parts of the FL cortex with
definable and segmentable margins in the T2-weighted
fluid-attenuated inversion recovery (FLAIR) sequence,
assessed by an experienced radiologist blinded to the
purpose of the study. For all analyses, a potential
edema zone was, if present, taken into account. Patients
with multifocal brain lesions, previous history of head
trauma or neurological disorders independent of brain
injury, signs of aphasia as well as presence of serious
functional impairments (i.e., patients with a Karnof-
sky index below 80%; Clark & Fallowfield, 1986)
were excluded. One patient had to be excluded due to
edema volume above 180 cm³. A second patient did
not complete the relevant assessment instruments. The
remaining fifteen patients took part in the analysis (M
age = 44.60 ± 8.22 years; range = 32–61; M lesion vol-
ume = 37.84 ± 34.84; range = 3.08 – 110.45; M years
since onset = 4.67 ± 3.81; range = 2–15). From the 15
patients, 10 were free of tumor recurrence and 5 had 1–3
tumor recurrence in the same lesion site. Twenty-nine
HC volunteers were recruited through advertisements
posted in newspapers, and were matched as closely
as possible to the patients for sex and age. Two
control participants had to be excluded because of
technical problems during the task. Three other par-
ticipants showed neurological abnormalities (signs
of microangiopathy, white matter lesion >1 cm, and
hematoma) and were also excluded. A participant could
not complete the Go/NoGo task, and was therefore
excluded. Another participant was excluded as well
due to heightened depression symptoms. The remain-
ing twenty-two HC volunteers (M age = 39.86 ± 11.44
years; age range = 23–59) without a history of neurolog-
ical or psychiatric disorders took part of the analysis. All
participants had normal or corrected vision and hear-
ing. Included FL patient’s characteristics are depicted
in Table 1.
From the FL-damaged patients, six patients had low-
grade (WHO◦ II; Kleihues & Sobin, 2000) and eight had
high-grade (WHO◦ III-IV) tumors. All patients under-
went biopsy (n = 3) or maximum safe resection (n = 11),
followed by radio- and/or chemotherapy. One patient
with a cyst involving grey matter of prefrontal cortex
was also included in the lesion group. Three lesions
did also include temporal and parietal regions. Lesion
volume was calculated using OsiriX software (Rosset,
Spadola, & Ratib, 2004). Taking edemas into account,
no lesion was bigger than 110 cm3.
All participants were informed about the risks of
the study and signed a written informed consent prior
91
to participation. This research was conducted with the
approval of the ethical board of the University of Hei-
delberg according to the declaration of Helsinki.
2.2. Neuropsychological and affective assessment
All participants completed a brief screening of cog-
nitive abilities. The Trail-Making-Test (TMT; Reitan,
1955) was used to assess cognitive flexibility in order
to control for possible differences between patients and
control, as well as memory performance (immediate
and delayed), which was assessed by the cognitive sub-
tests of the German Aphasia Checklist (ACL; Kalbe,
Reinhold, Ender, & Kessler, 2002). Response inhibi-
tion was measured using the computerized Go/NoGo
task of the German Test for Attentional Performance
(TAP 2.3, Psytest; Zimmermann & Fimm, 2002). This
task requires participants to respond to a Go stimulus,
an x, by pressing a button, while inhibiting the response
to a visually similar NoGo stimulus, a + sign. Task com-
pletion took 15 min, including practice trials. Number
of Errors (NoE) and reaction times (RT) were recorded.
The Becks Depression Symptom Inventory (BDI-II;
Kuhner, Burger, Keller, & Hautzinger, 2007) was used
for the assessment of depressive symptoms. In order to
assess the use of cognitive emotion regulation strate-
gies, the German version of the Cognitive Emotion
Regulation Questionnaire (CERQ; Garnefski & Kraaij,
2007; Loch, Hiller, & Witthoft, 2011) was employed.
This questionnaire presents 27 items in total, which
build nine subscales including self-blame, other-blame,
rumination, positive reappraisal, putting into perspec-
tive, acceptance, planning and positive refocusing. The
subscales measure emotion regulation behavior after a
negative event. Subscales of strategies shown to have
negative or positive outcomes in the long term can
also be calculated using combined scores of self-blame,
other-blame, rumination and catastrophizing as “mal-
adaptive” strategies, whereas reappraisal, putting into
perspective, acceptance, planning and positive refo-
cusing can be summarized as “adaptive” strategies
(Aldao et al., 2010).
2.3. Procedure
Given that the participants were originally recruited
for functional MRI assessments, they were invited for
two experimental sessions (cognitive and affective test-
ing and fMRI). The current study focuses only in the
first, testing session. This session included the neu-
ropsychological and affective assessment.
92 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients

Table 1
Included frontal lobe damaged patients
N. Sex Age Histopathology Years post onset Lesion side Lesion location Grading Approximate lesion volume (cm³)
1 f 42 Resected∗ 15 left frontotemporal WHO◦ II 3.47
Meningioma
2 f 38 Resected∗∗ 5 left frontal WHO◦ III 76.82
Oligodendroglioma
3 m 46 Resected∗∗ 7 right frontotemporo-parietal WHO◦ III 70.02
Oligoastrocytoma
4 m 46 Resected∗∗ 6 left frontal WHO◦ III 39.98
Oligoastrocytoma
5 f 40 Astrozytoma 2 right frontal WHO◦ II 5.67
6 m 55 Resected∗∗ 3 bilateral frontal WHO◦ III 90.09
Oligodendroglioma
7 f 52 Resected∗∗ 2 right frontal WHO◦ IV 46.53
Glioblastoma
8 f 61 Resected∗∗ 2 left frontal WHO◦ IV 14.56
Glioblastoma
9 m 32 Astrocytoma 2 left frontal WHO◦ II 9.58
10 m 32 Resected∗∗ 3 left frontoparietal WHO◦ II 11.61
Astrocytoma
11 f 45 Resected∗∗ 2 right frontal WHO◦ III 49.32
Oligodendroglioma
12 f 51 Resected∗∗ 4 right frontal WHO◦ II 15.74
Astrocytoma
13 m 43 Astrocytoma 2 right frontal WHO◦ II 20.47
14 m 49 Resected∗∗ 11 bilateral frontal WHO◦ III 110.45
Oligodendroglioma
15 f 37 Cyst 4 right frontal – 3.08
∗ Resectionmeans a complete removal of the neoplastic tissue, ∗∗ Resection is a macroscopic resection with at least microscopic neoplastic tissue
remaining in all cases.

2.4. Data analysis
First, the statistical distributions of all variables were
examined in both groups. The NoE of the Go/NoGo task
was not normally distributed. Therefore, square root
transformations were computed for this mostly skewed
variable, yielding values between 0 and 3 (Feilhauer,
Cima, Korebrits, & Kunert, 2012). The median RT of
the Go/NoGo task was used for analysis, following rec-
ommendations from the authors of TAP (Zimmermann
& Fimm, 2002).
Second, we computed combined mean scores for
maladaptive (self-blame, cathastrophizing, rumination
and other-blame) and adaptive (positive reappraisal,
putting into perspective, positive refocusing, refocus
on planning, acceptance) strategies of the CERQ and
examined whether these scores were significantly dif-
ferent between the frontal lobe patient group and the
healthy controls.
Third, we conducted a mediation analysis with
the group (dummy coded: 1 = FL patients, 0 = HC)
as the independent variable, the combined score of
maladaptive strategies as the dependent variable and
the squared-root corrected number of errors of the
Go/NoGo task as the mediator using the PROCESS tool
for SPSS with a 1000 bootstrapping algorithm media-
tion (Hayes, 2012).
3. Results
Statistical group differences in all measurements
are presented in Table 2. Regarding educational level,
50.0% of the patient sample and 46.7% of the HC sam-
ple had a college degree.
Given that radiotherapy might constitute a con-
founder regarding cognitive impairments and daily
functioning due to potential induced diffuse tis-
sue damage (Costello, Shallice, Gullan, & Beaney,
2004; Kangas, Tate, Williams, & Smee, 2012; Walter,
2010), we further examined the differences between
patients that received radiotherapy (n = 7) and patients
without radiotherapy (n = 8). A t-test for indepen-
dent groups revealed no significant differences in
depressive symptoms [t(13) = 0.82; p = 0.43], response
inhibition [t(13) = 0.08; p = 0.94], cognitive flexibil-
ity [t(13) = –1.48; p = 0.16] or memory performance
during immediate [t(13) = 1.63; p = 0.13] and delayed
recall [t(8.56) = 1.50; p = 0.17]. Furthermore, patients
 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients 93

Table 2
Demographic data and cognitive screening
Mean (SD) p Cohen’s d
FL-damaged (n = 15) HC (n = 22)
Age (years) 44.60 (8.22) 39.86 (11.45) 0.15 0.48
Educational Status 5.6 (2.72) 7 (1.38) 0.08 0.65
Depressive symptoms (BDI) 12.13 (8.68) 2 (2.83) <0.01 1.57
Memory Performance (ACL)
Immediate Memory 4.67 (1.23) 5.59 (0.73) <0.05 0.91
Delayed Memory 4.73 (1.44) 5.64 (0.66) <0.05 0.81
Cognitive Flexibility (Trail Making Task)
TMT A time (in sec) 24.90 (10.56) 18.40 (6.24) <0.05 0.75
TMT B time (in sec) 56.59 (22.08) 42.45 (11.76) <0.05 0.97
TMT time difference A - B 31.68 (14.66) 24.06 (10.79) 0.01 0.59
Behavioral Inhibition (Go/NoGo)
Median Reaction Time 399 (81.01) 420.09 (53.12) 0.39 0.31
Errors 1.93 (2.15) 0.36 (0.66) <0.05 0.99
SD = standard deviation, BDI = Becks Depression Inventory, ACL = aphasie check list.

did not differed significantly in the use of adap-
tive [t(13) = 1.23; p = 0.24] or maladaptive strategies
[t(13) = –0.41; p = 0.69].
The influence of tumor resection was also tested
by dividing the FL-damaged group into operated
patients (n = 11) and non-operated patients (n = 4).
Results of independent t-test revealed significant dif-
ferences in immediate memory recall [t(13) = 3.29;
p < 0.01], indicating that operated patients showed
more memory performance deficits in immediate
recalled items than non-operated patients. No signifi-
cant differences were found between groups regarding
depressive symptoms [t(13) = –0.77; p = 0.46], cogni-
tive flexibility [t(13) = 0.72; p = 0.48], delayed memory
recall [t(13) = 1.27; p = 0.23], response inhibition
[t(13) = –1.4; p = 0.17], as well as regarding adaptive
[t(13) = 0.007; p = 0.99] or maladaptive [t(13) = 0.89;
p = 0.39) strategies. Thus, as no significant influence
of radiotherapy or tumor resection on the variables of
interest (response inhibition, use of maladaptive strate-
gies) was found, these variables were not included in
the analysis.
As shown in Table 2, FL-damaged patients and
HC differed significantly in depressive symptoms
[t(16.05) = –4.37; p < 0.001], immediate [t(20.76) =
2.60; p = 0.02] and delayed memory scores
[t(18.03) = 2.28; p = 0.04] as well as in process-
ing speed during TMT performance (TMT-A: t(20.68);
p = 0.02, TMT-B: t(19.46); p = 0.04). Furthermore, in
line with our hypotheses, FL-damaged patients showed
more response inhibition deficits [t(35) = –3.89;
p < 0.01] and used more maladaptive strategies than
healthy participants [t(35) = –2.81; p < 0.01], as
depicted in Table 3. These differences where still
significant even after controlling for depression and
memory.
Hence, we examined the given Pearson’s correlations
for the primary variables of interest in the whole sample
(see Table 4). The higher the Go/NoGo error rate, the
higher the maladaptive CERQ score, r = 0.49, p = 0.002
as well as the depressive symptoms, r = 0.40, p = 0.02.
On the other hand, maladaptive strategy use showed
further significant positive correlations with processing
speed of TMT-A, r = 0.38, p = 0.02. So, in order to rule
out the influence of TMT-A differences between groups
on the use of maladaptive strategies, we performed a
partial correlation of group and maladaptive strategy
use controlling for this variable obtaining significant
results, r = 0.34, p = 0.05, which means that TMT-A pro-
cessing speed differences did not significantly influence
the differences between groups in the regular use of
maladaptive strategies.
Following, the mediation model of PROCESS for
indirect effects yielded significant results. First, group
categories predicted the use of maladaptive strategies
significantly, R2 = 0.18, β = 0.82, p = 0.008. Group cat-
egories were also a significant predictor for response
inhibition deficits (operationalized as squared-root
transformed Go/NoGo NoE), as the second regression
analysis showed, R2 = 0.30, β = 0.85, p < 0.001. In addi-
tion, the third regression analysis showed that response
inhibition deficits are a significant predictor for the use
of maladaptive strategies, R2 = 0.28, β = 0.46, p = 0.04,
as expected.
94 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients

Table 3
Cognitive emotion regulation strategies
Mean (SD) p Cohen’s d
FL-damaged (n = 15) HC (n = 22)
CERQ Subscales
Adaptive Scales
Acceptance 7.07 (2.96) 6.27 (2.76) 0.41 0.28
Positive reappraisal 5.80 (2.98) 6.41 (2.63) 0.52 0.22
Putting into perspective 5.87 (3.56) 6.23 (3.22) 0.75 0.11
Positive refocusing 6.00 (3.21) 4.18 (2.50) 0.06 0.63
Refocus on planning 7.73 (3.06) 7.82 (3.25) 0.94 0.03
Maladaptive Scales
Rumination 5.07 (2.34) 3.23 (1.90) <0.05 0.86
Self-blame 3.07 (1.83) 2.41 (1.56) 0.25 0.38
Cathastrophizing 2.93 (2.09) 1.36 (1.09) <0.05 0.94
Other-blame 1.20 (1.15) 1.95 (1.56) 0.12 0.55
Combined Scores
Adaptive strategies 6.49 (2.09) 6.18 (2.19) 0.67 0.14
Maladaptive strategies 3.07 (0.97) 2.24 (0.82) <0.01 0.92
HC: Healthy controls; FL: Frontal lobe patients; CERQ: Cognitive Emotion Regulation Questionnaire.

Table 4
Pearson’s correlation coefficients between variables of interest (N = 37)
1 2 3 4 5 6 7 8 9
1. Go/NoGo errors a) – 0.16 0.49∗∗ 0.40∗ 0.22 0.09 –0.03 –0.46∗∗ –0.29
2. Adaptive ER (CERQ)b) – 0.15 –0.05 0.01 0.06 0.08 0.05 0.12
3. Maladaptive ER (CERQ) – 0.29 0.38∗ 0.22 0.04 –0.16 –0.25
4. BDI – 0.36∗ 0.35∗ 0.24 –0.38∗ –0.49∗∗
5. TMT A time (in seconds) – 0.74∗∗ 0.34∗ –0.48∗∗ –0.30
6. TMT B time (in seconds) – 0.89∗∗ –0.35∗ –0.27
7. TMT B - TMT A – –0.16 –0.17
8. Immediate Memory – 0.68∗∗
9. Delayed Memory –
ER, Emotion Regulation; CERQ, Cognitive Emotion Regulation Questionnaire; BDI, Beck’s Depression Inventory; TMT; Trail-Making-Task,
∗∗ p < 0.01, ∗ p < 0.05, a) square-root transformed scores, b) combined scores of adaptive and maladaptive emotion regulation CERQ-scales.

Furthermore, there was a significant indirect effect
of FL-damage on the use of maladaptive strategies
through response inhibition, ß = 0.39, BCa CI [0.07,
0.94], showing that response inhibition fully mediated
the relationship between FL damage and maladaptive
ER. The beta values were significant with a medium to
large effect size of k2 = 0.18 (see Fig. 1).
4. Discussion
The goal of the present study was to explore the
impact of FL-damage on ER and the use of maladap-
tive strategies. As predicted, FL patients did use more
maladaptive ER strategies than HC. Furthermore, our
findings could show that response inhibition impair-
ments significantly mediate the use of maladaptive ER
strategies in FL patients, which suggests that deficits
inhibiting prepotent responses among FL patients might
explain the differences between FL-damaged patients
and HC in the use of maladaptive strategies. This find-
ing supports prior investigations linking maladaptive
strategy use with inhibition deficits (d’Acremont & Van
der Linden, 2007; Joormann & D’Avanzato, 2010) and
the ability to inhibit improper impulses to FL function
(Picton, et al., 2007).
Previous studies have already depicted a crucial neu-
ral interaction of frontal and subcortical systems for
the efficiency of ER, systems that overlap executive
functional areas (Goldin, McRae, Ramel, & Gross,
2008b; Ochsner, Bunge, Gross, & Gabrieli, 2002;
Ochsner, et al., 2004; Schulze, et al., 2011; Schweizer,
Grahn, Hampshire, Mobbs, & Dalgleish, 2013). The
present lesion study extend previous functional imag-
ing research by investigating the impact of FL lesions
on emotion regulation, showing that response inhibi-
tion deficits arising after FL damage might have a large
influence on emotion regulation behavior during nega-
tive emotional events. The use of maladaptive strategies
such as rumination has been previously linked with
 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients
Fig. 1. DE: direct effect, IE: Indirect effect; Figure shows the results of the mediation model. Response inhibition can be seen as a significant
mediator between FL-damage and maladaptive ER-strategies.
cognitive inhibition faculties (Joormann, 2010; Joor-
mann & Gotlib, 2010b; Zetsche, et al., 2012). Of crucial
importance for this view is the study of Joormann
and Gotlib (2008), linking rumination with inhibition
deficits and difficulties removing no longer relevant
cues from working memory (Joormann & Gotlib, 2008;
Joormann, Levens, & Gotlib, 2011). In contrast to cog-
nitive inhibition, response inhibition impairments not
only interfere with long-term emotion goals by fail-
ing to control impulsive needs, but also are related
to high levels of negative emotional reactivity (Hof-
mann et al., 2012; Leen-Feldner, Zvolensky, Feldner,
& Lejuez, 2004). For these reasons, the control of
impulsive responses might be an important predictor
for efficient regulation of automatically triggered emo-
tions. This assumption is supported by developmental
studies, which depicted that disinhibited children (i.e.,
impulsive, high in emotional intensity, and easily frus-
trated by failures) are considered poor in ER (Carlson
& Wang, 2007; Eisenberg & Morris, 2002; Eisenberg
& Sulik, 2012). Furthermore, a former study reported
that impulsivity can predict the use of maladaptive emo-
tion regulation strategies in adolescence (d’Acremont
& Van der Linden, 2007).
Surprisingly, however, the groups did not differ in the
use of adaptive ER strategies. We suggest two possi-
ble explanations to this finding. First, since FL patients
have difficulties controlling their impulses, they may
95
adopt every strategy, regardless of the situation. Second,
considering the life-struggling situation due to their
illness, patients might be confronted with several emo-
tions, and might be forced to learn and apply various
regulation strategies. Nevertheless, it has been argued
that adaptive strategies show weaker associations with
psychopathology compared to maladaptive strategies,
because their effective implementation is dependent
of contextual demands (contextual approach; Aldao &
Nolen-Hoeksema, 2012a). Therefore, even if the FL-
damaged patients use so much adaptive ER-strategies
as neurological healthy controls, it remains unclear
whether the used strategies are effective or implemented
in appropriate contexts. Further ER research dealing
with emotional regulatory behavior among brain lesion
patients should seek to manipulate context-relevant
cues or/and social feedback, which might be of particu-
lar importance for the interpretation of related cognitive
deficits among brain damaged patients.
Finally, we should consider some limitations. First,
CERQ does not include all regulation strategies, which
could be involved with inhibition (e.g., suppression).
Secondly, we did not manipulate context-related cues
in order to analyze appropriate vs. inappropriate strate-
gies. Other limitations include retrospective self-report
of ER behavior and heterogeneity of the FL-damaged
patient sample. Unfortunately, although we controlled
for radiotherapy and tumor resection effects, we cannot
96 R. Falquez et al. / Examining cognitive emotion regulation in frontal lobe patients
rule out effects of inter-individual cognitive deficits
within the small FL-lesion group (e.g., differences in
immediate memory recall), or the different influences
of slow-growing and fast-growing lesions (Desmur-
get, Bonnetblanc, & Duffau, 2007), so that our results
should be interpreted with caution. Further studies
should examine a larger, more homogeneous sample
of FL-damaged patients.
Considering these limitations, we believe is safe to
conclude that the findings of the current study support
the view that response inhibition impairments of FL-
damaged patients might strengthen the employment of
maladaptive strategies. Moreover, the stress produced
by the brain lesion and its impact in daily life cognitions
probably leads to more regulation needs. However, fur-
ther research should investigate whether the adaptive
strategies that arise from response inhibition deficits
are applied in the appropriate context.
Acknowledgments
This project was supported by the Neuro-oncology
section of the University Hospital and the German
Cancer Research Center in Heidelberg, Germany. The
authors are very thankful for the professional collabo-
ration of Dr. Benedikt Wiestler and Dr. Moritz Berger.
We would also like to thank Adelheid Fuxa and Moritz
Riese for their friendly assistance.
Conflict of interest
No conflict of interest disclosures are reported.
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