Neurological Research

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Anger and impulsiveness in migraine patients with

and without aura

Nermin Tanik, Tülin Akturk, Hikmet Saçmaci & Levent Ertugrul Inan

To cite this article: Nermin Tanik, Tülin Akturk, Hikmet Saçmaci & Levent Ertugrul Inan (2020):
Anger and impulsiveness in migraine patients with and without aura, Neurological Research, DOI:
10.1080/01616412.2020.1723974

To link to this article: https://doi.org/10.1080/01616412.2020.1723974

Published online: 05 Feb 2020.

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NEUROLOGICAL RESEARCH
https://doi.org/10.1080/01616412.2020.1723974

ARTICLE

Anger and impulsiveness in migraine patients with and without aura

a
Nermin Tanik , Tülin Akturka, Hikmet Saçmacia and Levent Ertugrul Inan a,b

a
Department of Neurology, Yozgat Bozok University Medical School, Yozgat, Turkey; bDepartment of Neurology, Ankara Research and
Training Hospital, Ankara, Turkey

ABSTRACT ARTICLE HISTORY

Background and purpose: Migraine is a common primary headache disorder triggered by Received 27 June 2019
internal or external stimuli. Impulsitivity and anger are associated with many neurological and Accepted 2 December 2019
psychiatric disorders. The aim of this study was to investigate the anger and impulsivity in KEYWORDS
migraine patients with or without aura. Migraine with aura; anger
Methods: A total of 55 patients aged between 18 and 55, who were diagnosed with episodic symptoms; impulsivity;
migraine (31 with aura and 24 without aura) and 40 healthy controls were enrolled in this female
prospective cross-sectional study.
Migraine diagnosis and classification were based on criteria from the International
Classification of Headache Disorders, 3rd edition (beta version). Multidimensional Anger
Scale and Barratt Impulsivity Scale-11 were administered to the patient and control groups.
Results:Migraine patients with aura, migraine patients without aura and control groups
were compared, anger symptoms were significantly higher in migraine patients with aura
(p < 0.001), but between these groups there was no significant difference in terms of impul-
sivity (p = 0.711).
Conclusions: It was found that anger symptoms were more common in migraine patients with
aura compared to migraine patients without aura and control group, but in impulsitivity there
was no difference between groups.
Further studies in future investigating the relation between migraine with aura and anger
may pave the way for different and more specified treatment approach.

Introduction in their ability to control and express anger. In addi-

Migraine is a primary headache that affects women
more often than men and is the sixth most common
cause of disability worldwide [1]. Typically, it is pre-
sented with acute symptoms and the mechanisms of
the disease seem quite complex. An important aspect
of migraine heterogeneity is its comorbidity with psy-
chiatric disorders. The most common psychiatric dis-
orders observed in this population are major
depression and anxiety. In migraine patients with
aura psychiatric comorbidity is more common than
those migraine patients without aura [2].
Anger and impulsivity are two social emotions that
determine a person’s propensity towards violence.
Anger is an emotion that occurs in situations such as
frustration, criticism and injustice and is necessary for
people to protect themselves. Impulsivity is one of the
sources of anger, associated with inhibition difficulties
and is a complex construct characterized by the ten-
dency to respond to internal or external stimuli with-
out assessing potential negative consequences [3].
Anger and impulsivity vary between individuals,
anger varies also by gender. Researchers showed that
men express their anger directly and women express
indirectly [4]. Patients suffering from headache have
been shown to suppress their anger, have impairment
tion, anger has been shown to correlate with depres-
sion and anxiety in patients with headache [5]. Only
a limited number of studies on anger and impulsivity
in migraine patients have been reported in the litera-
ture [6–8].
In this study, we aimed to investigate anger and
impulsivity in women patients with migraine with or
without aura. To our knowledge, this has not been
previously mentioned in the literature.
Methods
Study population
A total of 95 women (aged 18–55 years), composing of
55 migraine patients (31 migraine with aura, 24
migraine without aura) who applied to Neurology
outpatient clinic and 40 healthy controls were
included in this prospective and cross-sectional
study. Migraine diagnosis and classification were eval-
uated according to the beta version of International
Headache Classification 2013 [9].
Persons with neurological and psychiatric disor-
ders, those with limited ability to understand or
respond to any substance in the questionnaire intel-
lectually, and those who use drugs that affect the

CONTACT Nermin Tanik drnermin27@hotmail.com Department of Neurology, Yozgat Bozok University Medical School, Yozgat 66200, Turkey
© 2020 Informa UK Limited, trading as Taylor & Francis Group
2 N. TANIK ET AL.
central nervous system, including drugs used for
migraine prophylaxis, were not included in the
study. Detailed anamnesis was obtained from
migraine patients. Systemic physical examination and
neurological examination were performed. All
patients were examined at a time without headache.
The severity, frequency and duration of migraine
episode and the duration of the disease were recorded.
Visual analogue scale (VAS) was used to measure
severity of headache: 1–3: mild; 4–6: moderate; 7–8:
severe; 9–10: extremely severe [10]. Migraine head-
ache episode frequency was recorded monthly.
Headache episode durations were determined as
hours and duration of illness as years. Aura, photo-
phobia, osmophobia and phonophobia existence were
evaluated. Height and weight measurements were
recorded and body mass index (BMI) was calcu-
lated [11].
The Bozok University School of Medicine Ethics
Committee approved the study protocol (protocol
number:21.04.2014/49) and all the participants pro-
vided written informed consent.
Psychological tools
Multidimensional anger scale (MAS)
It is a battery consisting of 5 sections aimed at deter-
mining the feelings, thoughts and attitudes of people
on anger [12]. This scale consists of 158 items. All
items are scored between 1 and 5. It is expected that
one of the answers to the questions asked will be given
‘none’, ‘rarely’, ‘occasionally’, ‘frequently’ and ‘always’.
Calm behaviors subscale scores are not included when
the total scores of behaviors related to anger are taken.
High scores from the scale mean that the relevant
dimension is being used more.
(1) Section: Anger symptoms: ‘When you are
angry, how often do you have the following
symptoms?’ question is asked and a total of 14
items are given and the physical description of
the anger is tried to be determined.
(2) Section: Anger-eliciting situations: A total of 41
expressions are listed under the headings of
being belittled, being transgressed, being criti-
cized, which cause the formation of the anger,
and they are asked how much anger these
expressions have caused.
(3) Section: Anger-related cognitions: In this sec-
tion, consisting of a total of 30 items under the
main headings of regarding anger, regarding
others, regarding him or herself, and referring
to the whole world, ‘How often do the following
thoughts pass through your mind?’ Question is
asked.
(4) Section: Behaviors related to anger: There are 26
statements under the main headings of
aggressive behaviors, calm behaviors and
anxious behaviors ‘How often do you show the
following behaviors when you are in a situation
that makes you angry?’ question is asked.
(5) Section: Interpersonal anger: There are 47
questions under the headings of being revenge-
ful, passive-aggressive reactions, closing-in
reactions, being indifferent and answer to the
question of “‘How often do you show the fol-
lowing behaviours against a person who tempts
you?’ is sought.
When the other anger scales are taken into considera-
tion, the size of this scale is higher. Other anger scales
include 1 or 2 of these dimensions.
Barratt impulsiveness scale-11 (BIS-11)
It is a self-assessment scale consisting of 30 items
developed to measure impulsivity [13]. All items are
rated between 1 and 4 points. (1 = Rarely/Never, 2 =
Occasionally, 3 = Frequently, 4 = Almost always/
Always). There are three sub-scales in it.
(1) Attentional impulsiveness: Shows intolerance
to cognitive complexity and impatience.
(2) Motor impulsiveness: Shows instantly getting
into action without thinking.
(3) Non-planning impulsiveness: Represents the
absence of future feeling.
The higher the total BIS-11 score, the higher the
impulsivity level of the patient. The Turkish validity
and reliability study of BIS-11 was performed by Gülec
et al. [14].
Statistics
Analyses were conducted using the SPSS software (ver.
15.0, SPSS Inc., Chicago, IL, USA). A value of p < 0.05
was regarded as significant in all statistical analyses.
Descriptive analyses were presented using mean ± SD
for normally distributed and median 25–75th percen-
tiles for the non-normally distributed variables.
Number of cases and percentages were used for cate-
gorical data. A Kolmogorov–Smirnov test, histograms,
and q–q plots were used to test the normality of the
data, and Levene’s test was used to assess variance
homogeneity. Independent-sample t tests and Mann–
Whitney U tests were used to compare differences
between continuous variables, and chi-square (χ 2)
test was used in the analysis of categorical data.
Statistical difference between the groups in terms of
continuous variables was used One-way ANOVA for
parametric variables and Kruskall–Wallis test for non-
parametric variables. Post-hoc testing was performed
where the overall significance of the One-way
ANOVA or Kruskall–Wallis test was significant
(p < 0.05).
 NEUROLOGICAL RESEARCH 3

Table 1. Demographic and clinical features of the migraine patients and controls.
Control With aura Without aura
Variables (n = 40) (n = 31) (n = 24) p df F/Z/χ2
Age (years)* 35.6 ± 5.9 37 ± 9.1 37.2 ± 8.5 0.652 2 0.430
BMI (kg/m2)** 26.7 (23.8–28.2) 27.1 (22.6–29.6) 25.7 (22.4–32.2) 0.872 2 0.274
Attack severity*** - 7 (7–8) 8 (7–8) 0.824 −0.223
Attack frequency*** - 3 (2–4) 3 (2–4) 0.433 −0.785
Attack duration*** - 12 (8–24) 12 (8–24) 0.665 −0.433
Disease duration**** - 6.6 ± 4.5 6.6 ± 3.2 0.991 53 1.505
Photophobia***** - 29 (93.5)/2 (6.5) 22 (91.7)/2 (8.3) 0.791 1
Phonophobia***** - 30 (96.8)/1 (3.2) 21 (87.5)/3 (12.5) 0.186 1
Osmophobia***** - 26 (83.9)/5 (16.1) 20 (83.3)/4 (16.7) 0.957 1
*One-way ANOVA (F), mean ± SD **Kruskal–Wallis test (χ2), median (25–75th percentiles)
***Mann–Whitney U test (Z), median (25–75th percentiles) **** Independent-sample t test (F), mean ± SD
*****Chi-square test, values are expressed as n (%)
BMI, Body Mass Index; df, degrees of freedom.

Result migraine patients (with and without aura) and con-

Demographic and clinical features of the migraine
patients and controls are summarized in Table 1. No
significant difference was found between the groups
with respect to age or BMI (p > 0.05). Headache
characteristics, including attack severity, frequency
and duration, disease duration and photophobia, pho-
nophobia, osmophobia results were similar between in
migraineurs with or without aura (p > 0.05).
MAS (anger symptoms, anger-eliciting situations,
anger-related cognitions, behaviors related to anger,
interpersonal anger) scores of the migraine patients
(with and without aura) and controls are shown in
Table 2. Scores of anger symptoms were significantly
higher in the migraine with aura than in migraine with-
out aura and the control (p < 0.001). There were not
any significant differences in scores of anger-eliciting
situations, anger-related cognitions, behaviours related
to anger, interpersonal anger between in migraineurs
with or without aura and control (p > 0.05).
BIS-11 (attentional impulsiveness, motor impul-
siveness, non-planning impulsiveness) scores of the
trols are shown in Table 3. Similarly, there were not
any significant differences in scores of BIS-11 total,
attentional impulsiveness, motor impulsiveness and
non-planning impulsiveness between in migraineurs
with or without aura and control (p > 0.05).
Discussion
Two important findings emerged from this study.
First; anger symptoms of migraine patients with aura
were significantly higher than migraine patients with-
out aura and control group. Latter; there was no dif-
ference in impulsivity between migraine with aura,
migraine without aura and control group.
Studies on anger in migraine patients have shown
that these patients were over controller, experienced
anger without a specific provocation, anger was
a personality trait and they suppressed their anger
[5,15]. We also know that there is a correlation
between anger and anxiety. As a result of clinical
observations, it was shown that individuals with high

Table 2. Multidimensional anger scale scores in migraine patients and in controls.

Control With aura Without aura
Variables (n = 40) (n = 31) (n = 24) p df F/ χ2
Anger symptoms* 31.2 ± 9 40.8 ± 8.4 35.7 ± 10.6 <0.001 2 9.143
Anger-eliciting situations* (total) 157.8 ± 30.7 163.3 ± 26.5 170.8 ± 31.5 0.239 2 1.452
-Being belittled** 77 (56-86.5) 80 (72-90) 78.5(55.7-88) 0.150 2 3.797
-Being transgressed** 69 (63-74) 73 (67-76) 67(60.2-73.5) 0.091 2 4.791
-Being criticized** 18(15.2-21.7) 20 (18-23) 20 (17-23) 0.174 2 3.502
Anger-related cognitions* (total) 62.5 ± 16.3 65.8 ± 23 60.5 ± 16 0.569 2 0.568
-Regarding anger** 15.5(12.2-21) 17 (12-24) 17.5(12.5-23) 0.762 2 0.544
-Regarding others* 19.3 ± 5.9 19 ± 7.2 18 ± 4.7 0.712 2 0.341
-Regarding him or herself* 14.5 ± 3.5 16 ± 5.6 13.3 ± 4 0.085 2 2.536
-Regarding whole world** 10.5(8-15) 10(8-16) 11(7.2-14) 0.952 2 0.099
Behaviors related to anger* (total) 35.7 ± 10.2 35 ± 11.2 35.2 ± 9.1 0.955 2 0.046
-Aggressive behaviors** 20(18-29) 21 (16-30) 21.5(17.2-26) 0.842 2 0.345
-Calm behaviors* 33.2 ± 6.1 32.2 ± 8.5 31 ± 7.5 0.517 2 0.664
-Anxious behaviors* 12.3 ± 3.5 12.4 ± 3.7 11.7 ± 3.9 0.779 2 0.250
Interpersonal anger
-Being revengeful* 51.5 ± 21.3 45.9 ± 18.1 40.5 ± 12.5 0.068 2 2.773
-Closing-in reactions* 31 ± 6.2 32 ± 5.6 29.4 ± 7 0.319 2 1.158
-Passive-aggressive reactions* 29.2 ± 8.9 25.3 ± 9 24.6 ± 8 0.074 2 2.685
-Being indifferent* 7 ± 2.5 6±2 7.3 ± 3 0.116 2 2.202
*One-way ANOVA test (F), mean ± SD **Kruskal–Wallis test (χ2), median (25–75th percentiles)
df, degrees of freedom
4 N. TANIK ET AL.
Table 3. Barratt impulsiveness scale-11 scores in migraine patients and in controls.
Control
Variables aura (n = 40)
Total* 57.1 ± 7.4
Attentional impulsiveness* 15 ± 2.4
Motor impulsiveness** 17 (16-19)
Non-planning impulsiveness* 24.4 ± 3.9
*One-way ANOVA test (F), mean ± SD **Kruskal–Wallis test (χ2), median (25–75th percentiles)
df, degrees of freedom
anxiety could not express their anger easily and anger
suppression was associated with anxiety personality
traits [16]. Patients with headache have a tendency to
experience anger even without specific provocation,
and the tendency to express this anger internally or
externally is associated with anxiety. It is known that
migraine patients experience anxiety after expressing
their anger [6].
Although migraine patients are generally known to
have an angry temperament, anger symptoms of
migraine patients with aura (being told to himself,
loss of control, feeling blood rushing to the brain,
clenching fists, clenching teeth, brain throbbing,
hand and foot trembling, acceleration of movement,
shortness of breath, headache, breathing through the
nose, thinking irrationally, biting lips) were not well
known. Symptomatology and characteristics of
migraine focus on generalized neuronal hyperexcit-
ability due to genetic predisposition [17]. Migraine
aura is caused by waves of cortical spreading depres-
sion. Although specific processes that initiate cortical
spreading depression in humans are unknown, emo-
tional or physiological stress, such as lack of sleep, may
play a role in this stage. However, there is an alter-
native hypothesis that the aura does not begin as
a result of cortical spreading depression. According
to this hypothesis; locally released serotonin nitric
oxide as a result of platelet aggregation causes the
release of calcitonin gene – related peptide. A high
concentration of serotonin can induce slow calcium
waves in gap-junction astrocyte syncytium. This pro-
cess was responsible for the aura symptoms, which
progressed slowly [18]. According to the generally
accepted opinion: Aura is presumably a hereditary
cortical hyperexitability [19]. Studies have reported
that hyperexcitability is more common in migraine
with aura than without aura. Studies have reported
that hyperexcitability is more common in migraine
with aura than without aura [20–22]. Amplitude of
the resting state functional magnetic rezonanse ima-
ging activity was higher in migraine patients with aura
than migraine without aura [20]. Visual evoked poten-
tial (VEP) responses indicated that hyperexcitability
was more commonly expected in migraine with aura.
A significant increase in VEP amplitudes (P1N2 and
N1P1) was observed in migraine patients with aura
than those without aura [21]. Abnormal cortical excit-
ability affects more commonly migraine patients with
With aura Without
(n = 31) (n = 24) p df F/ χ2
56.7 ± 7.4 58.6 ± 6.6 0.592 2 0.527
14.2 ± 3.8 15 ± 3.4 0.577 2 0.553
18 (15-20) 17.5 (15-20.7) 0.999 2 0.003
24.5 ± 3.6 25.7 ± 3.3 0.367 2 1.012
aura and increased cortical excitability is in multisen-
sor interactions [22].
As in migraine with aura, there are studies showing
that the brain is in a hyperexcitable state during anger.
Increased motor corticospinal excitability was deter-
mined at the time of anger with transcranial magnetic
stimulation [23]. In another study higher amplitudes of
VEP was recorded in response to anger as was in
migraine with aura [24]. In a research on neuroanatomy
of anger, temporal pole was found to be important in
expression and control of anger [25]. In migraine
patients, hyperexcitability of the temporal pole – ante-
rior temporal pole in particular-in interictal period [26]
during attacks [27] and in migraine visual aura [28] has
been shown. Temporal lobe hyperexcitability has been
shown in migraine in a study [29].
One reason for why migraine patients with aura hav-
ing intense anger symptoms is that migraine and anger
are linked with each other in terms of hyperexcitability,
additionally, we also think that hyperexcitability of the
temporal pole in interictal period, during attacks and in
migraine aura may contribute these symptoms. We have
been confronted by a chicken and egg dilemma and
actually we do not know which comes first; the hyper-
excitability or the anger. A question in our mind; may
waves of cortical spreading depression be a part of anger?
Another reason for anger in migraine patients with
aura may be low levels of serotonin. Serotonin is one of
the key neurotransmitters for migraine and plasma ser-
otonin levels have been found to be low during migraine
attacks [30]. Plasma serotonin level in migraine patients
with aura has been lower than in migraine patients with-
out aura, a study by Nagata et al. [31]. A neurochemical
study on anger has revealed that there is a relation
between anger and central serotonergic dysregulation
[32]. Polymorphism of the gene coding for tryptophan
hydroxylase (TPH), the rate-limiting enzyme in seroto-
nin biosynthesis, resulted in low levels of serotonin
which was associated with anger-related personality traits
[33]. The limbic system is believed to play an important
role in the perception of migraine especially in the amyg-
dala and hippocampus [34]. The amygdala, which com-
bines information from cortical and thalamic sensory
inputs, leads to anxiety-related behaviors. Low serotonin
is known to play a role in anxiety disorders [35,36]. It has
been found that 5- hydroxytryptamine (5-HT) in the
amygdala regulates anxiety responses by activating
5-HT1A receptors [37]. Considering that serotonin levels

are lower in migraine patients with aura according to the
patients migraine without aura, we can presume that
anxiety disorders may be seen more frequently in
migraine patients with aura. In another study, it was
shown that those with U allele in TPH gene have anger-
related features [38].
Impulsivity is a psychological phenomenon that has
not been extensively studied in headache patients. It is
modulated by serotonin and has a strong hereditary
component [39]. Associations between BIS total score
and various aspects of the serotonin system were deter-
mined. Most of the genetic association studies focused
on serotonergic polymorphism [40]. A relation between
TPH genotype and impulsivity has been determined
[41]. There is evidence that low levels of serotonin
neurotransmission were associated with increased
impulsivity [42]. As we mentioned above, plasma ser-
otonin level in migraine patients with aura has been
lower than in migraine patients without aura [31].
Studies on impulsivity in migraine patients are limited.
In a study assessing impulsivity among patients with
chronic migraine; no correlation has been found
between chronic migraine and impulsivity [7]. In
another study including migraineurs and tension head-
ache patients; migraineurs have been found to have
a higher level of impulsivity than tension headache
patients [8]. There might be two reasons for the detec-
tion of higher levels of impulsivity in migraine patients
in that study. First of all, there was no control group and
migraine patients had higher impulsivity levels than
tension headache patients. Secondly, both female and
male migraine patients were included in that study. In
our study, we included only female patients with episo-
dic migraine. Inclusion of the male patients may have
affected the outcomes of the mentioned study.
We did not find any difference in impulsivity
between migraine with aura, migraine without aura
and control groups. There may be several reasons for
this. Firstly; serotonergic hypofunction may present
various features depending on several factors such as
receptors of serotonergic agents (ex; receptor type),
type of impulsive behaviour and genetic combination
(ex; serotonergic system and other neurotransmitter
systems) [43]. In addition, inclusion of only female
patients may also have affected the results of this
study. Because genetic influence on impulsivity is
affected by gender. Genetic influences are slightly
stronger in males than in females [44]. In a study by
Evans et al., impulsivity was found to be associated
with the TPH gene in men [45]. In addition, disin-
hibition levels are higher in boys than in girls [46].
Our study had some limitations. First of all,
a methodological problem is that, this is a cross-
sectional study and since it is not a longitudinal
study, it may be difficult to establish a causal relation-
ship. Secondly, we did not include male patients and
chronic migraineurs, but anger and impulsivity may
NEUROLOGICAL RESEARCH 5
vary depending on gender and chronicization of
migraine. Finally, scales are based on the patient’s self-
report; therefore, there are always possibilities of irre-
levant or misleading answers.
In conclusion, despite limitations, this is the first study
showing that in migraine patients with aura the anger
response is significantly higher than migraineurs without
aura and than control group but there was no difference
in impulsivity. Understanding the psychiatric correla-
tions of migraine patients with aura is critical.
Moreover, to improve patients’ insight into their anger
responses and to increase skills in coping will contribute
to the treatment.
Further studies in more detail on anger responses of
migraine patients with aura will help to better under-
standing the pathophysiology and may contribute to the
development of different treatment protocols specific to
the disease.
Disclosure statement
No potential conflict of interest was reported by the authors.
Notes on contributors
Nermin Tanik is association professor in Department of
Neurology at Yozgat Bozok University Medical School.
Her research focused on headache and smell. Tanık has
published articles in leading journals.
Tülin Akturk is an assistant professor in Neurology depart-
ment, at Yozgat Bozok University. Her researches have
mainly focused on migraine, primary headaches, cognition
and neurotoxicity. In addition to these Akturk has published
articles in few journals.
Hikmet Saçmaci is an assistant professor in Neurology
department, at Yozgat Bozok University. Her researches
have mainly focused on migraine, primary headaches, neu-
rophsiology and multiple sclerosis. In addition to these
Saçmacı has published articles in few journals.
Levent Ertugrul Inan is professor in Department of
Neurology at Ankara Research and Training Hospital. He
is interested in headache and cognitive behavioral
therapy. Inan has many publications about headache in
leading journals.
ORCID
Nermin Tanik http://orcid.org/0000-0002-7567-9244
Levent Ertugrul Inan http://orcid.org/0000-0002-2441-
0624
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