Professional Documents
Culture Documents
Content Server
Content Server
Introduction
Benzodiazepine (BZD) abuse is a growing worldwide problem in light of the addictive
potential of these drugs and its effect on the impairment of functional outcome (Lader,
2011; Lalive, Rudolph, Lüscher, & Tan, 2011). BZDs are widely prescribed for the
treatment of anxiety, insomnia and panic disorder, depression and social phobia, as
well as in the management of withdrawal symptoms (Lalive et al., 2011; Latt, Coni-
grave, Marshall, Saunders, & Nutt, 2009). BZDs have a strong depressant effect on
the central nervous system (CNS) with outcomes ranging from mild sedation
through to coma (Barker, Greenwood, Jackson, & Crowe, 2004). A study using neu-
ropsychological and electroencephalography (EEG) methods conducted on healthy vol-
unteers established that even small-dose BZD intake may significantly impair not only
perceptual and motor processes but has the potential to also affect complex cognitive
functions, such as the ability to implement novel rules (Muñoz-Torres, Armony, Trejo-
Martínez, Conde, & Corsi-Cabrera, 2011; Muñoz-Torres, del Río-Portilla, & Corsi-
Cabrera, 2011). Other research shows that BZD intake negatively affects processing
speed, working and episodic memory (Carter, Griffiths, & Mintzer, 2009; Loring
et al., 2011) as well as attention vigilance, startle response (Murphy, Downham,
Cowen, & Harmer, 2008), and intellectual ability (Paraherakis, Charney, & Gill,
2001). The study conducted by Boeuf-Cazou, Bongue, Ansiau, Marquié, and
Lapeyre-Mestre (2011) found that long-term BZD use adversely affects long-term
memory in women, whereas a meta-analysis of cognitive outcome of long-term BZD
use found impairments across all 12 tested domains irrespective of sex, i.e., in
sensory processing, psychomotor speed, non-verbal memory, visuospatial, processing
speed, problem-solving, attention, verbal memory, general intelligence, motor
control, working memory, and verbal reasoning (Barker et al., 2004).
Cognitive dysfunction related to visual attention, task switching and motor response in
patients addicted to BZD may decrease through detoxification (Kałwa, 2014a, 2014b).
Therefore, the time of testing may affect performance and a cognitive improvement can
be detected shortly after detoxification. BZD in-patient detoxification is carried out in
four stages (Basińska-Starzycka, Jamroży, & Habrat, 2009). In the first phase, diazepam
substitution prevents severe withdrawal symptoms. The drug concentration level is
tested daily in the blood and cumulates at the satiation level after diazepam substitution.
During the second stage, diazepam doses are reduced and the drug concentration level is
systematically decreased until full BZD elimination from the blood. The fourth stage con-
sists of monitoring the patient’s adaptation to complete BZD elimination. The whole
process takes approximately 6–8 weeks.
The prevalent reasons behind BZD use are “emotional” in character, e.g., “nervous-
ness” and “worries” related to family, financial, day-to-day coping, as well as existential
issues (Alvarenga, Giacomin, De Loyola, Uchoa, & Firmo, 2014). Studies show that
BZD dependence affects mostly women. BZD users are characterised by a high level
of anxiety, tension, and introversion, as well as a diminished capacity to experience
pleasure (Konopka, Pełka-Wysiecka, Grzywacz, & Samochowiec, 2013; Krawczyk,
Lelek, Mróz, Kamenczak, & Chrostek-Maj, 2009). It has also been found that BZD
users score higher on the Beck Depression Inventory and are significantly more dis-
tressed than alcoholics and cocaine users (Paraherakis et al., 2001). BZDs affect
mood through their anxiolytic and sedative effect (Curran, 1991). They have also
been found to affect the ability to recognise emotional facial expressions in healthy
individuals, particularly anger (Blair & Curran, 1999) and fear (Coupland, Singh,
Sustrik, Tink, & Blair, 2003; Zangara, Blair, & Curran, 2002). These results are incon-
sistent with the findings of a study conducted by Kamboj and Curran (2006) which
recorded no impairments in facial emotion recognition tasks. This may perhaps be
explained by the selected methodology which consisted of morphed grayscale images
of the most confused basic emotions (happiness was morphed with surprise, surprise
with fear, fear with sadness, sadness with disgust, and disgust with anger) and the
76 N. ŻUROWSKA ET AL.
participants were all young healthy individuals with a mean age of 25 ± 4. The authors
also used lorazepam in place of diazepam used in a previous study (Blair & Curran,
1999) as well as in other studies (Coupland et al., 2003). The critical literature
review conducted by Sabino, Chagas, and Osório (2016) on the recognition of facial
expressions of emotion (RFEE) in the treatment of anxiety disorders provides a sys-
tematic overview of the effect of different drugs on RFEE. Studies selected focused
on trials on healthy individuals as opposed to the current study which investigates a
clinical population of long-term users. Furthermore, the selected studies used static
stimuli in their RFEE tasks. The authors conclude that selective serotonin reuptake
inhibitors have the opposite effect on RFEE tasks compared to BZD. They also stipulate
that reduced fear recognition related to BZD (particularly diazepam) may be explained
by their effect on GABAergic receptors in the amygdala, namely the reduced reactivity
of the amygdala when presented with expressions of fear.
Furthermore, there is some evidence that BZD promotes antisocial behaviour and
facilitate violent criminal behaviour (Dåderman, Fredriksson, Nilsson, Kristiansson, &
Lidberg, 2004). Accordingly, there is an assumption based on an animal study on rats
that these drugs may inhibit empathic responses (Ben-Ami Bartal et al., 2016).
Conversely, it has been shown that in healthy men a dose of 25 mg oxazepam did not
reduce empathy for pain (Nilsonne et al., 2017). However, authors concluded that a higher
dose of the drug would have inhibited empathic responding. Other studies indicate that
drug addicted (Ferrari, Smeraldi, Bottero, & Politi, 2014), as well alcohol-dependent sub-
jects (Maurage et al., 2011) exhibit an impairment mainly of the cognitive aspect of
empathy.
Given these inconsistent results, the aim of the present study was to investigate whether
and, if so, how deeply, BZD affects aspects of social cognition. We tested the recognition
and intensity rating of emotional facial expressions (joy, anger, sadness, and fear) as well as
empathy which, similarly to facial emotion recognition, is a relevant factor of social
cognition.
All subjects in the experimental groups were tested either during diazepam intake or
following diazepam elimination from the blood. We chose natural facial expressions in
both static and dynamic form from the Amsterdam Dynamic Facial Expression Set
(ADFES) (Van der Schalk, Hawk, Fischer, & Doosje, 2011) in light of studies showing
that dynamic stimuli promote recognition accuracy and are a truer reflection of real-life
situations (Rymarczyk, Żurawski, Jankowiak-Siuda, & Szatkowska, 2016a, 2016b; Traut-
mann, Fehr, & Herrmann, 2009). The stimuli were selected in a way as to present the
emotions in the most discernible way. Thereby any differences in recognition accuracy
could be interpreted as to indicate a clear impairment in facial emotion recognition.
Empathy levels were scored with the short version of the Empathy Quotient (EQ-Short)
which measures empathy across three domains: cognitive empathy, affective empathy,
and social functioning (Baron-Cohen & Wheelwright, 2004; Jankowiak-Siuda, Rymarczyk,
& Grabowska, 2011; Wakabayashi et al., 2006). We hypothesised that BZD dependence
impairs facial emotion recognition accuracy, particularly in static stimuli. However, we
predicted an improvement after detoxification. Consistently with studies on empathy
and addiction conducted on patients detoxifying through diazepam substitution
(Ferrari et al., 2014; Maurage et al., 2011), we hypothesised lower EQ scores in the exper-
imental groups compared to the control group.
COGNITIVE NEUROPSYCHIATRY 77
performance on the testing procedures. This group included seven women and six men
with an average age of 46.38 years (SD = 14.64). Seven persons declared having secondary
education and six declared having higher education. The average addiction period in this
group was 8.77 years (SD = 6.81) and the most recent average BZD concentration in the
blood prior to testing amounted to 476.31 ng/ml (SD = 536.89). The BZD concentrations
tested in the blood varied severely between subjects owing to differing doses used prior to
detoxification as well as metabolism rates. Seven persons described their mood as negative,
four as neutral, and two as positive.
The second clinical group (N = 15) was tested after completion of the detoxification
procedure with no BZD presence tested in the blood. Subjects were controlled for post-
withdrawal symptoms that could affect their results. This group consisted of 11 women
and 4 men averaging 56.47 years in age (SD = 11.65) and an average period of BZD use
of 8.53 years (SD = 5.76). One person declared having primary education, whereas second-
ary and higher education was declared equally among the remaining group subjects. Mood
was rated negative by five persons, neutral by four, and positive by six subjects.
The demographically matched control group consisted of healthy subjects who were
interviewed prior to the testing procedures in order to exclude any participants under-
going treatment with psychotropic drugs with special emphasis on BZD use. The
control group did not present with any psychiatric, neurologic, or somatic symptoms
during testing. Participants for the control group (N = 15) were recruited from the
general population. Subjects in this group were naive to BZDs. This group consisted of
eight women and seven men with an average age of 45.93 years (SD = 9.22). Six
persons declared having a secondary level of education, whereas the rest declared
having a higher level of education. Eight participants rated their mood as neutral with
the remaining stating a positive mood.
Assessments
Empathy levels were measured with the short version of the EQ (Wakabayashi et al.,
2006), originally developed by Baron-Cohen and Wheelwright (2004). The EQ-Short con-
sists of 22 statements related to the ability to recognise other people’s thoughts and feelings
known as mentalization, as well as emotional responses to them. The standardised Polish
translation of the EQ was used in this study (Jankowiak-Siuda et al., 2017).
Emotion recognition accuracy was measured with a computerised emotion recognition
task prepared using E-Prime 2.0 software and stimuli from the ADFES (Van der Schalk
et al., 2011). Four female and four male actors were selected from the stimulus database
expressing four emotions (joy, anger, sadness, and fear) in both static (photo) and
dynamic (video) modality (see Figure 1). A total of 64 stimuli were displayed during
the facial emotion task. All selected stimuli consisted of white actors in light of evidence
of an in-group facial recognition bias (Kaspar, 2016).
The dynamic stimuli consisted of 4s facial expression sequences from neutral
expression to apex (100% intensity), whereas the static stimuli consisted of a 4s display
of the emotion expression apex at 100% intensity. Thereby, both the static and dynamic
stimuli were displayed for the same duration. The long presentation time was also
meant to facilitate recognition. Any recognition errors could then be analysed as to indi-
cate severity of impairment owing to either BZD use or to pre-existing cognitive
COGNITIVE NEUROPSYCHIATRY 79
Figure 1. Examples of static stimuli selected for the computerized RFEE task (fear, anger, sadness, and
joy) from the ADFES database.
Results
Data were analysed in SPSS 23pl. An intergroup univariate analysis with the Bonferroni
correction established that the groups differ in age (F(2, 40) = 3.68; p < .05). However,
post hoc analysis with Bonferroni correction found only a statistical tendency (p = .058)
whereby the second clinical group is older than the control group. The experimental
groups did not differ in terms of addiction period.
Table 2. Differences in accuracy scores by emotion and modality between the investigated groups.
Group 1 Group 2
Substitution Post- Group 3
treatment detoxification Control
M SE M SE M SE F (df) p
Joy 0.99 .01 0.97 .01 0.99 .01 2.52 (6, 111) <.05a
Sadness 0.85 .04 0.82 .04 0.97 .03 NS
Fear 0.82 .04 0.80 .05 0.96 .04 <.05b
Anger 0.90 .02 0.94 .02 0.97 .02 <.05b
<.05c
Static modality 0.86 .03 0.87 .03 0.96 .02 7.87 (1, 37) <.01a
Dynamic modality 0.91 .02 0.89 .02 0.98 .01
Overall recognition accuracy 0.89 .02 0.88 .02 0.97 .02 8.30 (2, 37) <.01a
<.01c
<.001b
NSd
Notes: Accuracy was scored as (1—correct; 0—incorrect). The recognition scores for the different emotions show the
overall score of accuracy for both static and dynamic stimuli representing that emotion.
Statistical significance of differences:
a
Main effect significance.
b
Between post-detoxification (group 2) and controls (group 3).
c
Between substitution treatment (group 1) and controls (group 3).
d
Between substitution treatment (group 1) and post-detoxification (group 2).
COGNITIVE NEUROPSYCHIATRY 81
Analysis further provided a significant interaction between the factors emotion and
group (F(6, 111) = 2.51; p < .05). Post hoc tests with the Bonferroni correction showed
that the post-detoxification group (M = 0.82; SE = .04; p < .05) was less accurate in recog-
nising sadness than the control group (M = 0.97; SE = .03). The post-detoxification group
(M = 0.80; SE = .05; p < .05) was also less accurate in recognising fear compared to the
control group (M = 0.96; SE = .02), whereas the substitution treatment group (M = 0.90;
SE = .20; p < .05) was less accurate in recognising anger than the control group (M = 0.97;
SE = .02). Furthermore, the control group was equally accurate in recognising the respective
emotions. Differences in recognition accuracy between the emotions were found only in the
experimental groups with joy being the emotion with the highest recognition accuracy.
The substitution treatment group was more accurate in recognising joy (M = 0.99; SE
= .01) than any other emotion, i.e., sadness (M = 0.85; SE = .04; p < .01), fear (M = 0.82;
SE = .04; p < .01), or anger (M = 0.90; SE = .20; p < .01). In the post-detoxification group,
joy (M = 0.97; SE = .01) was significantly better recognised than sadness (M = 0.82; SE
= .04; p < .05) and fear (M = 0.80; SE = .05; p < .05). Similarly, anger (M = 0.94; SE = .02)
was more accurately recognised than sadness (p < .05) and fear (p < .05) in the post-detox-
ification group.
The factors emotion and gender significantly interacted with each other (F(3, 111) =
3.07; p < .05). Men (M = 0.94; SE = .03). Men were more accurate than women (M = 0.82;
SE = .03) in recognising sadness (p < .01). Women were most accurate in recognising joy
(M = 9.8; SE = .01) which proved easier to recognise than sadness (M = 0.82; SE = .03;
p < .001), fear (M = 0.84; SE = .03; p < .001), and anger (M = 0.92; SE = .01; p < .01).
The recognition of sadness among women was also less accurate than that of anger
(p < .01). Again, this result should be viewed with caution in light of the limited
sample size.
Table 3. EQ scores.
Group 1
Substitution Group 2 Group 3
treatment Post-detoxification Control F (df) p
M SD M SD M SD 0.24(2.40) NS
43.00 10.78 45.60 12.12 43.67 8.22
Male (N = 17) Female (N = 26) t (df) p
M SD M SD 2.38 (41) <.05
47.00 11.01 39.76 7.43
Discussion
The aim of our study was to assess the effect of BZD use and detoxification on facial
emotion recognition and empathy which represent aspects of emotional and social cogni-
tion processes. We found significant differences in emotion recognition accuracy between
individuals addicted to BZD and healthy controls with no differences in the intensity
rating of emotional facial expressions and the EQ. Our results in the scope of RFEE
agree with those of previous studies, in which BZD impaired the subjects’ ability to recog-
nise emotional expressions (Blair & Curran, 1999; Coupland et al., 2003; Zangara et al.,
2002). Similar results were found in patients addicted to alcohol who, compared to
healthy controls, showed a decreased ability to read emotions from human faces
(Farges et al., 2004; Maurage et al., 2011). However, it is worth emphasising that the
results of facial expression recognition in patients addicted to alcohol are rather inconsist-
ent and generally contradictory albeit with a trend towards deficits in RFEE among alco-
holics (for review see Donadon & de Lima Osório 2014).
In our study, we found that the decreased ability to recognise emotions in individuals
addicted to BZD was particularly related to negative emotions of fear, sadness, and anger
with no differences in the recognition of joy. This result might be attributed to the effect of
contrast as joy was the only positive emotion presented to subjects and is also reflected in
the review by Sabino et al. (2016) who found that most studies of RFEE with BZD users
showed no impairment in the recognition of joy. Similar results were found by Khawar,
Malik, Maqsood, Yasmin, and Habib (2013) in whose study joy was also the most accu-
rately recognised, whereas fear proved the most difficult. Our findings of negative
emotion recognition impairment are also consistent with other research showing a diaze-
pam-induced lower recognition accuracy of anger (Blair & Curran, 1999) and fear (Coup-
land et al., 2003; Zangara et al., 2002). These results may be a diazepam-specific effect as
research conducted by Kamboj and Curran (2006) showed no emotion recognition
impairment after lorazepam intake. This differentiation has also been pointed out by
Sabino et al. (2016) who attribute the impaired recognition of fear and anger to the
acute anxiolytic effect of BZD, most notably diazepam, and their effect on the GABAergic
receptors of the amygdala responsible for the processing of fear.
Furthermore, some research shows that age is a predictor of recognition accuracy
(Donadon & de Lima Osório, 2014; Thompson & Voyer, 2014; Weidner, 2014).
Khawar et al. (2013) found that fear is more difficult to discern from 40 years of age
and anger from the age of 50 years. In our study, the participants’ average age was
above 40 years with the second group showing a tendency to be older than the control
group. Despite the fact that all participants fell within the age in which recognition
COGNITIVE NEUROPSYCHIATRY 83
accuracy had been proven to be reduced, only the experimental groups exhibited signifi-
cant impairments in recognition accuracy between the emotions. It can be hypothesised
that age was not a predictor of accuracy in our study pointing to a more probable
impact of BZDs, notably diazepam, on the established differences. The process of detox-
ification involves long-term acting BZD substitution with diazepam which is then system-
atically reduced. Therefore, all investigated patients were tested during or right after
diazepam substitution.
In our study, facial emotion recognition accuracy between the sexes varies depending
on the group being investigated. We found that BZD users, particularly women, exhibit
an impairment in the ability to correctly identify negative emotions from facial
expressions. Despite this finding, EQ scores were higher in women than in men in the
investigated samples which follow the conventional understanding that women are
more “emotional” than men (Kring & Gordon, 1998). Recently, Hall, Hutton, and
Morgan (2010) discussed this notion from the evolutionary perspective explaining that,
as mothers, women are more sensitive to non-verbal expressions. Furthermore, some
studies showed that women scored higher than males on self-report empathy scales
(Baron-Cohen & Wheelwright, 2004; Davis, 1996). However, the discussion continues
on whether female superiority in empathy would be confirmed using more objective
measures of empathic abilities (Rueckert, Branch, & Doan, 2011). In our study, although
the EQ was higher in women, men were significantly more accurate in reading emotions
from faces, particularly in recognising sadness. Similar results were found in the study of
Kessler, Roth, Von Wietersheim, Deighton, and Traue (2007) who investigated the influ-
ence of panic disorder on the recognition of six basic emotions. As in the present study,
more women than men composed the investigated group (78%). However, the established
differences in recognising sadness and anger in favour of men became less significant in
that study when researchers took into account the intensity of symptoms of depression
and anxiety that were higher in women. These factors were not controlled for in this
study and therefore our results should be viewed in light of both this limitation as well
as with caution to the small sample size. It can, however, be hypothesised based on the
results of quoted studies that factors other than sex may be stronger predictors of the
ability to correctly identify facial expressions of emotion.
Our next goal was to assess the impact of BZD on empathy. We found no significant
differences in empathy scores between clinical subjects and controls. There is an ongoing
debate regarding the emphatic abilities of BZD users (Nilsonne et al., 2017). It seems that
in drug (Ferrari et al., 2014) or alcohol users (Maurage et al., 2011), the main deficits
concern emotional, not cognitive empathy. In our study, we used EQ-Short scale which
assesses the general level of empathy. It is possible that a more specific tool targeting
emotional empathy would reveal some deficit in BZD users compared to controls.
Further research is warranted in this respect.
In terms of the detoxification effect, our research found that the post-detoxification
group (testing negative for BZD in the blood) did not show any significant differences
in reading emotions compared to individuals that were still in substitution treatment.
This suggests that the impairment of the ability to recognise emotions in BZD abusers
might be a long-term effect. The diminished ability to recognise emotional facial
expressions in both groups can also be partly explained by CNS disinhibition caused by
BZD withdrawal. According to Latt et al. (2009), the process of detoxification can give
84 N. ŻUROWSKA ET AL.
more severe symptoms than addiction, e.g., increased anxiety, which may in turn impact
on general emotional outcome. Our findings should be treated with caution in light of this
study’s limitations. We investigated relatively small groups and we did not control for
depressive and anxiety symptoms. Apart from obtaining an opinion from the consulting
psychiatrist describing withdrawal symptoms as low before proceeding with the test pro-
cedures, we did not perform any assessment of withdrawal syndrome intensity. Further
studies are necessary to investigate patients with BZD addiction and withdrawal to
better understand the nature of their diminished ability to read emotions from faces.
Finally, in our study both static (photo) and dynamic (video) emotional stimuli were
used. In terms of the impact of stimulus modality, consistently with other findings
(Donadon & de Lima Osório, 2014; Rymarczyk et al., 2016a; Trautmann et al., 2009)
dynamics improved recognition accuracy owing to its higher ecological validity.
However, only in the group starting detoxification were dynamic stimuli better recognised
than static stimuli, albeit with the reservation that there was no significant group ×
modality effect. Perhaps in this group of individuals information from dynamic facial
expressions proved helpful to emotion recognition and static emotions were more difficult
to discern without the dynamic context. The above hypotheses, however, should be inves-
tigated by further studies.
In conclusion, to our knowledge, the present study is the first that investigates the
empathic abilities as well the ability to recognise emotions from faces in patients not
only addicted to but also detoxified from BZD drugs. Despite the limitations of the pre-
sented study, it seems that our results may be useful to help us better understand the
social cognition processes of BZD users and to contribute to the development of effective
interventions based on the ways in which patients with BZD dependence perceive their
social environment.
Acknowledgements
The authors would like to thank the clinical staff of the detoxification and withdrawal
symptoms management ward of the Institute of Psychiatry and Neurology in Warsaw,
and, particularly, the clinical director of the ward Anna Basińska-Szafrańska MD PhD,
without whose ongoing support this research would not have been possible.
Disclosure statement
No potential conflict of interest was reported by the authors.
References
Alvarenga, J. M., Giacomin, K. C., De Loyola, A. I., Uchoa, F. E., & Firmo, J. O. A. (2014). Chronic
use of benzodiazepines among older adults. Revista de Saúde Pública, 48(6), 866–872. doi:10.
1590/S0034-8910.2014048004986
Barker, M. J., Greenwood, K. M., Jackson, M., & Crowe, S. F. (2004). Cognitive effects of long-term
benzodiazepine use. CNS Drugs, 18(1), 37–48. doi:10.2165/00023210-200418010-00004
Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient: An investigation of adults with
Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism
and Developmental Disorders, 34(2), 163–175. doi:10.1023/B:JADD.0000022607.19833.00
COGNITIVE NEUROPSYCHIATRY 85
Basińska-Starzycka, A., Jamroży, A., & Habrat, B. (2009). Odstawianie benzodiazepin i leczenie
zespołów abstynencyjnych u osób uzależnionych—indywidualizacja postępowania w oparciu o
monitoring kliniczny i farmakokinetyczny [Benzodiazepine discontinuation and withdrawal
treatment individualization of treatment based on using clinical assessment and pharmacoki-
netic monitoring]. Alkoholizm i Narkomania, 22(1), 75–86.
Ben-Ami Bartal, I., Shan, H. Z., Molasky, N. M. R., Murray, T. M., Williams, J. Z., Decety, J., &
Mason, P. (2016). Anxiolytic treatment impairs helping behavior in rats. Frontiers in
Psychology, 7, 19. doi:10.3389/fpsyg.2016.00850
Blair, R. J. R., & Curran, H. V. (1999). Selective impairment in the recognition of anger induced by
diazepam. Psychopharmacology, 147, 335–338. doi:10.1007/s002130051177
Boeuf-Cazou, O., Bongue, B., Ansiau, D., Marquié, J., & Lapeyre-Mestre, M. (2011). Impact of long-
term benzodiazepine use on cognitive functioning in young adults: The VISAT cohort. European
Journal of Clinical Pharmacology, 67(10), 1045–1052. doi:10.1007/s00228-011-1047-y
Carter, L. P., Griffiths, R. R., & Mintzer, M. Z. (2009). Cognitive, psychomotor, and subjective
effects of sodium oxybate and triazolam in healthy volunteers. Psychopharmacology, 206(1),
141–154. doi:10.1007/s00213-009-1589-1
Coupland, N. J., Singh, A. J., Sustrik, R. A., Tink, P., & Blair, R. J. (2003). Effects of diazepam on
facial emotion recognition. Journal of Psychiatry and Neuroscience, 28(6), 452–463.
Curran, H. V. (1991). Benzodiazepines, memory and mood: A review. Psychopharmacology, 105(1),
1–8. doi:10.1007/BF02316856
Dåderman, A. M., Fredriksson, B., Nilsson, L. H., Kristiansson, M., & Lidberg, L. (2004). The abuse
of a sleeping pill that contains the active substance flunitrazepam (FZ)—for example, Rohypnol
—and the effects of FZ intoxication, such as enhanced violence and disturbed memory. Journal of
the American Academy of Psychiatry Law Online, 32(4), 467–468.
Davis, M. H. (1996). Empathy: A social psychological approach. Boulder, CO: Westview Press.
Donadon, M. F., & de Lima Osório, F. (2014). Recognition of facial expressions by alcoholic
patients: A systematic literature review. Neuropsychiatric Disease and Treatment, 1655–1663.
doi:10.2147/NDT.S65376
Farges, F., Corcos, M., Speranza, G., Loas, F., Perez-Diaz, F., Venisse, J. L., … Jeammet, P. (2004).
Alexithymie et toxicomanie: lien avec la dépression. L’Encéphale, 30, 201–211. doi:10.1016/
S0013-7006(04)95431-0
Ferrari, V., Smeraldi, E., Bottero, G., & Politi, E. (2014). Addiction and empathy: A preliminary
analysis. Neurological Sciences, 35(6), 855-859. doi:10.1007/s10072-013-1611-6
Hall, J. K., Hutton, S. B., & Morgan, M. J. (2010). Sex differences in scanning faces: Does attention to
the eyes explain female superiority in facial expression recognition? Cognition and Emotion, 24
(4), 629–637. doi:10.1080/02699930902906882
Jankowiak-Siuda, K., Kantor-Martynuska, B., Siwy-Hudowska, A., Śmieja, M., Dobrołowicz-
Konkol, M., Zaraś-Wieczorek, I., & Siedler, A. (2017). Psychometric properties of a Polish adap-
tation of short form of the Empathy Quotient (EQ-Short). Psychiatria Polska, 51(4), 197–734.
doi:10.12740/PP/64270
Jankowiak-Siuda, K., Rymarczyk, K., & Grabowska, A. (2011). How we empathize with others: A
neurobiological perspective. Medical Science Monitor, 17(1), RA18–RA24. doi:10.12659/MSM.
881324
Kałwa, A. (2014a). Changes in cognitive function during benzodiazepine withdrawal. European
Neuropsychopharmacology, 24(S2), S684.
Kałwa, A. (2014b). Changes in cognitive functions during benzodiazepine discontinuation in
women. Biological Psychiatry, 75(9S), 208.
Kamboj, S. K., & Curran, H. V. (2006). Scopolamine induces impairments in the recognition of
human facial expressions of anger and disgust. Psychopharmacology, 185(4), 529–535. doi:10.
1007/s00213-006-0332-4
Kaspar, K. (2016). Culture, group membership, and face recognition. Commentary: Will you
remember me? Cultural differences in own-group face recognition biases. Frontiers in
Psychology, 7, 1101. Retrieved from http://doi.org/10.3389/fpsyg.2016.01101
86 N. ŻUROWSKA ET AL.
Kessler, H., Roth, J., Von Wietersheim, J., Deighton, R. M., & Traue, H. C. (2007). Emotion recog-
nition patterns in patients with panic disorder. Depression and Anxiety, 24(3), 223–226. doi:10.
1002/da.20223
Khawar, R., Malik, F., Maqsood, S., Yasmin, T., & Habib, S. (2013). Age and gender differences in
emotion recognition ability and intellectual functioning. Journal of Behavioural Sciences, 23(3),
53–71.
Konopka, A., Pełka-Wysiecka, J., Grzywacz, A., & Samochowiec, J. (2013). Psychosocial character-
istics of benzodiazepine addicts compared to not addicted benzodiazepine users. Progress in
Neuro-Psychopharmacology and Biological Psychiatry, 40, 229–235. doi:10.1016/j.pnpbp.2012.
09.001
Krawczyk, E., Lelek, A., Mróz, S., Kamenczak, A., & Chrostek-Maj, J. (2009). Regulacja stanów
emocjonalnych u pacjentów uzależnionych od benzodiazepin—doniesienia wstępne
[Emotional regulations among benzodiazepines dependent patients preliminary results].
Przegląd Lekarski, 66(6), 315–318.
Kring, A. M., & Gordon, A. H. (1998). Sex differences in emotion: Expression, experience, and
physiology. Journal of Personality and Social Psychology, 74, 686–703. doi:10.1037//0022-3514.
74.3.686 PMID: 9523412
Lader, M. (2011). Benzodiazepines revisited—will we ever learn? Addiction, 106(12), 2086–2109.
doi:10.1111/j.1360-0443.2011.03563.x
Lalive, A. L., Rudolph, U., Lüscher, C., & Tan, K. R. (2011). Is there a way to curb benzodiazepine
addiction? Swiss Medical Weekly, 141, w13277. doi:10.4414/smw.2011.13277
Latt, N., Conigrave, K., Marshall, J., Saunders, J., & Nutt, D. (Eds.) (2009). Addiction medicine (pp.
168–184). Oxford: Oxford University Press.
Loring, D. W., Marino, S. E., Drane, D. L., Parfitt, D., Finney, G. R., & Meador, K. J. (2011).
Lorazepam effects on word memory test performance: A randomized, double-blind, placebo-
controlled, crossover trial. The Clinical Neuropsychologist, 25(5), 799–811. doi:10.1080/
13854046.2011.583279
Maurage, P., Grynberg, D., Noël, X., Joassin, F., Philippot, P., Hanak, C., … Campanella, S. (2011).
Dissociation between affective and cognitive empathy in alcoholism: A specific deficit for the
emotional dimension. Alcoholism: Clinical & Experimental Research, 35(9), 1–7.
Muñoz-Torres, Z., Armony, J. L., Trejo-Martínez, D., Conde, R., & Corsi-Cabrera, M. (2011a).
Behavioural and neural effects of diazepam on a rule-guided response selection task.
Neuroscience Research, 70(3), 260–268. doi:10.1016/j.neures.2011.03.009
Muñoz-Torres, Z., del Río-Portilla, Y., & Corsi-Cabrera, M. (2011b). Diazepam-induced changes in
EEG oscillations during performance of a sustained attention task. Journal of Clinical
Neurophysiology, 28(4), 394–399. doi:10.1097/WNP.0b013e318227323a
Murphy, S., Downham, C., Cowen, P., & Harmer, C. (2008). Direct effects of diazepam on
emotional processing in healthy volunteers. Psychopharmacology, 199(4), 503–513. doi:10.
1007/s00213-008-1082-2
Nilsonne, G., Tamm, S., Golkar, A., Sörman, K., Howner, K., Kristiansson, M., … Petrovic, P.
(2017). Effects of 25 mg oxazepam on emotional mimicry and empathy for pain: A randomized
controlled experiment. Royal Society Open Science, 4, 160607. http://dx.doi.org/10.1098/rsos.
160607
Paraherakis, A., Charney, D., & Gill, K. (2001). Neuropsychological functioning in substance-
dependent patients. Substance Use & Misuse, 36(3), 257. doi:10.1081/JA-100102625
Rueckert, L., Branch, B., & Doan, T. (2011). Are gender differences in empathy due to differences in
emotional reactivity? Psychology, 2(6), 574–578. doi:10.4236/psych.2011.26088
Rymarczyk, K., Żurawski, Ł, Jankowiak-Siuda, K., & Szatkowska, I. (2016a). Do dynamic compared
to static facial expressions of happiness and anger reveal enhanced facial mimicry? PLoS ONE, 11
(7), e0158534. doi:10.1371/journal.pone.0158534
Rymarczyk, K., Żurawski, Ł, Jankowiak-Siuda, K., & Szatkowska, I. (2016b). Emotional empathy
and facial mimicry for static and dynamic facial expressions of fear and disgust. Frontiers in
Psychology, 7, 403. doi:10.3389/fpsyg.2016.01853
COGNITIVE NEUROPSYCHIATRY 87
Sabino, A. V., Chagas, M. N., & Osório, F. L. (2016). Effects of psychotropic drugs used in the treat-
ment of anxiety disorders on the recognition of facial expressions of emotion: Critical analysis of
literature. Neuroscience and Biobehavioral Reviews, 71, 802–809. doi:10.1016/j.neubiorev.2016.
10.027
Thompson, A. E., & Voyer, D. (2014). Sex differences in the ability to recognise non-verbal displays
of emotion: A meta-analysis. Cognition and Emotion, 28(7), 1164–1195. doi:10.1080/02699931.
2013.875889
Trautmann, S. A., Fehr, T., & Herrmann, M. (2009). Emotions in motion: Dynamic compared to
static facial expressions of disgust and happiness reveal more widespread emotion-specific acti-
vations. Brain Research, 1284, 100–115. doi:10.1016/j.brainres.2009.05.075
Van der Schalk, J., Hawk, S. T., Fischer, A. H., & Doosje, B. (2011). Moving faces, looking places:
Validation of the Amsterdam Dynamic Facial Expression Set (ADFES). Emotion, 11(4), 907–920.
doi:10.1037/a0023853
Wakabayashi, A., Baron-Cohen, S., Wheelwright, S., Goldenfeld, N., Delaney, J., & Fine, D. (2006).
Development of short forms of the Empathy Quotient (EQ-Short) and the Systemizing Quotient
(SQ-Short). Personality and Individual Differences, 41, 929–940. doi:10.1016/j.paid.2006.03.017
Weidner, K. E. (2014). Recognizing emotional faces: The role of gender, age, and attractiveness.
Dissertation Abstracts International, 74, 8-B(E).
Zangara, A., Blair, R., & Curran, V. H. (2002). A comparison of the effects of a β-adrenergic blocker
and a benzodiazepine upon the recognition of human facial expressions. Psychopharmacology,
163(1), 36–41. doi:10.1007/s00213-002-1120-4
Copyright of Cognitive Neuropsychiatry is the property of Taylor & Francis Ltd and its
content may not be copied or emailed to multiple sites or posted to a listserv without the
copyright holder's express written permission. However, users may print, download, or email
articles for individual use.