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COGNITIVE NEUROPSYCHIATRY, 2018

VOL. 23, NO. 2, 74–87


https://doi.org/10.1080/13546805.2018.1426448

Recognition of emotional facial expressions in benzodiazepine


dependence and detoxification
Natasza Żurowskaa, Agnieszka Kałwab, Krystyna Rymarczyka and Bogusław Habratc
a
Department of Experimental Psychology, Institute of Cognitive and Behavioural Neuroscience, University of
Social Sciences and Humanities, Warsaw, Poland; bDepartment of Child and Adolescence Psychiatry, Institute
of Psychiatry and Neurology, Warsaw, Poland; cDepartment of Prevention and Treatment for Addictions,
Institute of Psychiatry and Neurology, Warsaw, Poland

ABSTRACT ARTICLE HISTORY


Introduction: The study investigates how benzodiazepine (BZD) Received 2 August 2017
use and detoxification affects empathy and the recognition and Accepted 3 January 2018
intensity rating of emotional facial expressions. The sample
KEYWORDS
comprised 43 participants in three groups: (1) during Benzodiazepine use;
detoxification (N = 13), (2) after detoxification (N = 15), (3) a detoxification; empathy;
matched control group (N = 15). Clinical subjects were recruited emotion recognition
from in-patients of an addiction treatment unit.
Methods: Empathy levels were tested with the Empathy Quotient
(EQ-Short). Recognition accuracy and emotion intensity rating
were based on a computerised task displaying static and dynamic
facial expressions of joy, anger, sadness, and fear.
Results: The controls proved more accurate than both experimental
groups in identifying facial expressions of negative emotions. Joy
recognition proved most accurate overall. Among the clinical
subjects, women in particular exhibited an impaired ability to
correctly identify negative emotions from facial expressions.
Dynamic stimuli were better recognised than static ones albeit
only in the experimental groups. No significant differences were
found for emotion intensity ratings and EQ scores.
Conclusion: Our findings suggest that the impaired facial emotion
recognition accuracy is not caused by deficits in empathy. No
improvement was recorded post-detoxification which may
indicate impaired interpersonal functioning among BZD users.
Further research is warranted in light of this study’s limitations.

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

CONTACT Natasza Żurowska nzurowska@st.swps.edu.pl


© 2018 Informa UK Limited, trading as Taylor & Francis Group
COGNITIVE NEUROPSYCHIATRY 75

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

Material and methods


Participants and design
The present study analysed intergroup differences between three groups: two clinical
groups (group 1 consisting of subjects with during substitution treatment and group 2
of post-detoxification subjects with no BZD present in the blood) and a matched
control group (see Table 1). The clinical groups were recruited among in-patients of
the detoxification and withdrawal symptoms management ward of the Institute of Psy-
chiatry and Neurology in Warsaw admitted for detoxification from BZDs. The subjects
were diagnosed with mental and behavioural disorders related to the use of sedatives, hyp-
notics, anxiolytics, according to ICD-10 substance-use disorders criteria. The excluding
factors were: (1) dual diagnosis, i.e., other, besides BZD dependence, serious psychiatric
conditions (psychotic disorders, dissociative disorders, eating disorders, and bipolar dis-
order) as well as severe withdrawal symptoms associated with somatic (e.g., dizziness,
nausea, headache, other somatic complications) or psychiatric conditions (e.g., strong
anxiety) rendering study participation impossible, (2) multiple substance detoxification,
and (3) significant medical (chronic somatic illness or severe complications in the
course of withdrawal) and, particularly, neurologic disorders (e.g., head trauma, brain
tumour, neurological disorders, such as multiple sclerosis or Huntington’s disease). Par-
ticipants from the clinical groups were nominated by their consultant psychiatrist follow-
ing clinical assessment. The current detoxification status of patients was confirmed by
consulting psychiatrists in order to meet the inclusion criteria. All study subjects were
Caucasian and Polish-speaking. The study had the approval of the Ethical Committee
of the SWPS University of Social Sciences and Humanities in Warsaw, Poland, and was
conducted in accordance with the standards of the Helsinki Declaration on scientific
research on humans. All subjects gave written informed consent.
Demographic data were collected from all participants at the beginning of the test pro-
cedure and included: sex, age, education, mood, and—for the clinical groups—recent BZD
concentration in the blood and period of drug use prior to current hospitalisation (see
Table 1). Post hoc tests (Bonferroni correction) found that the post-detoxification group
tended to be older than the control group (p = .058). Mood was rated on a subjective
scale whereby the participants themselves declared if their mood can be rated negative,
neutral, or positive at the time of testing. The first clinical group (N = 13) consisted of sub-
jects tested upon admission or at any point during the substitution phase of the detoxifi-
cation procedure. The participants were nominated by their consultant psychiatrist and
were assessed as not exhibiting withdrawal symptoms that could adversely affect their

Table 1. Characteristic of sample.


Group (N = 43) Group 1 (N = 13) Group 2 (N = 15) Control Group 3 (N = 15)
Agea M SD M SD M SD
46.38 14.64 56.47 11.65 45.93 9.22
Sex Male Female Male Female Male Female
6 7 4 11 7 8
Period of BZD use M SD M SD M SD
pre-detoxification 8.77 6.81 8.53 5.76 N/A N/A
Education Primary Secondary Higher Primary Secondary Higher Primary Secondary Higher
0 7 6 1 7 7 0 6 9
a
Post hoc tests showed group 2 tends to be older than the control group (p = .058).
78 N. ŻUROWSKA ET AL.

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.

impairments of the studied sample depending on between group differences found. A 3s


fixation point was displayed prior to each stimulus. The stimuli were presented in a fixed
randomised order to all participants in a way ensuring that no stimulus characteristic
(actor gender, emotion type, modality type) was displayed more than twice in a row.
Stimulus presentation was immediately followed by two questions displayed one by one
with the second question being shown once response was given to the first one. The ques-
tions consisted of: (1) a forced-choice format question asking the subjects to name the
emotion with keyboard numbers being assigned to each emotion and (2) a question
graded on a five-point Likert scale asking the participants to assess the intensity of the dis-
played emotion (from 1—not intense to 5—very intense). The computerised procedure
design has been presented in Figure 2.
Stimuli were presented on the same computer monitor for all participants in daylight
conditions. All participants were tested at the same time of day. Subjects responded by press-
ing the relevant number key on the computer keyboard. Answers could not be changed nor
could the stimulus be replayed. Before the task, a test version consisting of one static and one
dynamic stimuli was run using actors not selected for the task procedure.

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.

Figure 2. Computerised task design.


80 N. ŻUROWSKA ET AL.

Emotion recognition accuracy


A mixed model ANOVA with the Bonferroni correction was calculated to examine recog-
nition accuracy. The within-subjects factors were the facial expressions (fear, anger,
sadness, joy) and modality (dynamic, static) whereas the between-subjects factors were
gender and group. One point was scored for accurate recognition and 0 was scored for
inaccurate recognition. The results have been presented in Table 2.
The results showed a significant group effect (F(2, 37) = 8.30; p < .01) whereby the sub-
stitution treatment group (M = 0.89; SE = .02; p < .01) and the post-detoxification group
(M = 0.88; SE = .02; p < .001) were overall less accurate in recognising facial expressions
of emotion than the control group (M = 0.97; SE = .02). There was no significant difference
in accuracy between the substitution treatment group and the post-detoxification group.
A main gender effect was also found (F(1, 37) = 4.43; p < .05) showing that men (M =
0.94; SE = .02) made less mistakes than women (M = 0.89; SE = .01; p < .05) when recog-
nising emotions. This result should be approached with caution in view of the limited
sample size.
A main modality effect was established (F(1, 37) = 7.87; p < .01) whereby dynamic
emotions (M = 0.93; SE = .01) were better recognised than static emotions (M = 0.90; SE
= .01). Although no significant interaction between group and stimulus modality was
found (F(2, 37) = 1.12; NS), an analysis of simple effects showed that only the substitution
treatment group was significantly more accurate in recognising dynamic stimuli than
static stimuli (p < .01).
The emotion factor also provided significant results (F(2.34, 86.57) = 10.51; p < .001).
Post hoc tests with Bonferroni correction showed that joy (M = 0.98; SE = .01) was more
accurately recognised than all other emotions, i.e., sadness (M = 0.88; SE = .02; p < .001),
fear (M = 0.86; SE = .03; p < .001), and anger (M = 0.94; SE = .01; p < .05). Moreover, fear
proved to be the least recognised emotion with significantly lower recognition accuracy
compared to both joy (p < .001) and anger (p < .05).

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.

Emotion intensity rating


A mixed model ANOVA was calculated to examine intensity ratings. No significant
differences between the studied groups were found. However, a significant emotion
effect was found (F(2.28, 84.20) = 12.36; p < .001) whereby the study subjects rated joy
(M = 3.60; SE = .12) as more intense than sadness (M = 3.15; SE = .11; p < .001) and
anger (M = 3.18; SE = .12; p < .01). Moreover, fear (M = 3.36; SE = .13) was seen as
more intense than sadness (M = 3.15; SE = .11; p < .05) and anger (M = 3.18; SE = .12;
p < .05). Analysis showed a significant modality effect (F(1, 37) = 5.16; p < .05)
whereby static facial expressions of emotion (M = 3.37; SE = .12) were rated as more
intense than dynamic expressions (M = 3.28; SE = .10). No significant gender effect
was found.

Empathy Quotient (EQ-Short)


A multivariate ANOVA was calculated with the factors group and gender to test for differ-
ences in EQ scores (see Table 3). The group factor proved insignificant. There was also no
significant interaction effect. A student’s t-test established a significant gender effect
(t(41) = 2.38; p < .05) whereby overall women (M = 47; SD = 11) scored higher than
men (M = 39.76; SD = 7.43; p < .05) on the empathy scale.
82 N. ŻUROWSKA ET AL.

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.

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