Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study
Emotional face recognition has been shown to be drastically impaired among patients with schizophrenia. Since the underlying processes of this deficit have not been widely addressed, we attempted to investigate the relationship between facial expression perception and clinical symptoms in patients...
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Інститут фізіології ім. О.О. Богомольця НАН України
2013
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| Цитувати: | Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study / M. Akbarfahimi, M. Tehrani-Doost, F. Ghassemi // Нейрофизиология. — 2013. — Т. 45, № 3. — С. 279-287. — Бібліогр.: 41 назв. — англ. |
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nasplib_isofts_kiev_ua-123456789-1481002025-02-09T20:55:08Z Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study Сприйняття емоційного виразу обличчя у пацієнтів, котрі страждають на шизофренію: дослідження з відведенням пов’язаних з подією еег-потенціалів Akbarfahimi, M. Tehrani-Doost, M. Ghassemi, F. Emotional face recognition has been shown to be drastically impaired among patients with schizophrenia. Since the underlying processes of this deficit have not been widely addressed, we attempted to investigate the relationship between facial expression perception and clinical symptoms in patients with schizophrenia. We enrolled 28 patients with schizophrenia and 28 healthy adults matched by their sex and age. The amplitude and latency of component N170 in event-related EEG potentials (ERPs) induced by presentations of happy, fearful, and neutral face images were comparatively evaluated in these two groups. Furthermore, the relationship between the N170 measures and clinical symptoms of schizophrenia were assessed using the Positive and Negative Syndrome Scale (PANSS). The N170 responses to facial expressions in patients with schizophrenia were significantly delayed, as compared to healthy control participants [F (1, 54) = 4.25, P = 0.044]. The N170 response to fearful faces (as compared to happy and neutral faces) was elicited with the minimum latency in the control group, while this component was most delayed among schizophrenics. Positive schizophrenia symptoms correlated with the amplitudes of the left-hemisphere N170 component in response to happy, fearful, and neutral faces. Our findings suggest that the facial expression deficit in schizophrenia is related to delayed responses in face perception and is influenced by the severity of positive symptoms. The evident delay in fearful face perception among patients with schizophrenia may partly explain their inappropriate reactions to threatening conditions. У пацієнтів, котрі страждають на шизофренію, розпізнавання виразів обличчя є серйозно порушеним. Оскільки процеси, що зумовлюють подібний дефіцит, вивчені недостатньо, ми намагалися дослідити співвідношення сприйняття виразів обличчя та клінічних симптомів у пацієнтів із цим захворюванням. В обстежувану групу ввійшли 28 пацієнтів із діагнозом шизофренія та 28 дорослих суб’єктів; групи були узгоджені в статевому та віковому аспектах. У представників цих двох груп вимірювали та порівнювали амплітуду й латентний період компонента N170 у складі пов’язаних з подією потенціалів, викликаних пред’явленням зображень облич зі щасливим, переляканим і нейтральним виразом. Потім оцінювали взаємозв’язок параметрів N170 з оцінками клінічних симптомів шизофренії згідно зі шкалою позитивних і негативних синдромів (PANSS). Розвиток компонента N170 після пред’явлення зображень облич з різними виразами відбувався у пацієнтів із шизофренією істотно пізніше, ніж у здорових контрольних суб’єктів [F (1, 54) = = 4.25, P = 0.044]. N170 після пред’явлення переляканих облич (порівняно зі щасливими та нейтральними) розвивався у суб’єктів контрольної групи з мінімальною затримкою, а у шизофреників він виникав значно пізніше. Інтенсивність позитивних симптомів у шизофреників корелювала з амплітудами N170 у лівій півкулі після пред’явлення як щасливих, так і переляканих і нейтральних облич. Наші спостереження показують, що дефектність сприйняття виразу обличчя у пацієнтів, хворих на шизофренію, пов’язана із затримкою відповідей ЦНС, і на таку дефектність впливає тяжкість позитивних симптомів. Очевидна затримка сприйняття облич з переляканим виразом у пацієнтів із шизофренією може частково пояснювати неадекватність їх реакцій на загрозливі ситуації. This study was a part of the first author’s thesis to obtain the PhD degree in cognitive neuroscience (brain and cognition) at the Institute for Cognitive Science Studies, Tehran, Iran. 2013 Article Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study / M. Akbarfahimi, M. Tehrani-Doost, F. Ghassemi // Нейрофизиология. — 2013. — Т. 45, № 3. — С. 279-287. — Бібліогр.: 41 назв. — англ. 0028-2561 https://nasplib.isofts.kiev.ua/handle/123456789/148100 612.822:547.918 en Нейрофизиология application/pdf Інститут фізіології ім. О.О. Богомольця НАН України |
| institution |
Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| collection |
DSpace DC |
| language |
English |
| description |
Emotional face recognition has been shown to be drastically impaired among patients with
schizophrenia. Since the underlying processes of this deficit have not been widely addressed,
we attempted to investigate the relationship between facial expression perception and clinical symptoms in patients with schizophrenia. We enrolled 28 patients with schizophrenia and
28 healthy adults matched by their sex and age. The amplitude and latency of component
N170 in event-related EEG potentials (ERPs) induced by presentations of happy, fearful, and
neutral face images were comparatively evaluated in these two groups. Furthermore, the relationship between the N170 measures and clinical symptoms of schizophrenia were assessed
using the Positive and Negative Syndrome Scale (PANSS). The N170 responses to facial
expressions in patients with schizophrenia were significantly delayed, as compared to healthy
control participants [F (1, 54) = 4.25, P = 0.044]. The N170 response to fearful faces (as
compared to happy and neutral faces) was elicited with the minimum latency in the control
group, while this component was most delayed among schizophrenics. Positive schizophrenia
symptoms correlated with the amplitudes of the left-hemisphere N170 component in response
to happy, fearful, and neutral faces. Our findings suggest that the facial expression deficit
in schizophrenia is related to delayed responses in face perception and is influenced by the
severity of positive symptoms. The evident delay in fearful face perception among patients
with schizophrenia may partly explain their inappropriate reactions to threatening conditions. |
| format |
Article |
| author |
Akbarfahimi, M. Tehrani-Doost, M. Ghassemi, F. |
| spellingShingle |
Akbarfahimi, M. Tehrani-Doost, M. Ghassemi, F. Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study Нейрофизиология |
| author_facet |
Akbarfahimi, M. Tehrani-Doost, M. Ghassemi, F. |
| author_sort |
Akbarfahimi, M. |
| title |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study |
| title_short |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study |
| title_full |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study |
| title_fullStr |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study |
| title_full_unstemmed |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study |
| title_sort |
emotional face perception in patients with schizophrenia: an event-related potential study |
| publisher |
Інститут фізіології ім. О.О. Богомольця НАН України |
| publishDate |
2013 |
| url |
https://nasplib.isofts.kiev.ua/handle/123456789/148100 |
| citation_txt |
Emotional Face Perception in Patients with Schizophrenia: an Event-Related Potential Study / M. Akbarfahimi, M. Tehrani-Doost, F. Ghassemi // Нейрофизиология. — 2013. — Т. 45, № 3. — С. 279-287. — Бібліогр.: 41 назв. — англ. |
| series |
Нейрофизиология |
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NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3 279
UDC 612.822:547.918
M. AKBARFAHIMI,1,2 M. TEHRANI-DOOST,3,1 and F. GHASSEMI4,1
EMOTIONAL FACE PERCEPTION IN PATIENTS WITH SCHIZOPHRENIA:
AN EVENT-RELATED POTENTIAL STUDY
Received December 15, 2012.
Emotional face recognition has been shown to be drastically impaired among patients with
schizophrenia. Since the underlying processes of this deficit have not been widely addressed,
we attempted to investigate the relationship between facial expression perception and clini-
cal symptoms in patients with schizophrenia. We enrolled 28 patients with schizophrenia and
28 healthy adults matched by their sex and age. The amplitude and latency of component
N170 in event-related EEG potentials (ERPs) induced by presentations of happy, fearful, and
neutral face images were comparatively evaluated in these two groups. Furthermore, the re-
lationship between the N170 measures and clinical symptoms of schizophrenia were assessed
using the Positive and Negative Syndrome Scale (PANSS). The N170 responses to facial
expressions in patients with schizophrenia were significantly delayed, as compared to healthy
control participants [F (1, 54) = 4.25, P = 0.044]. The N170 response to fearful faces (as
compared to happy and neutral faces) was elicited with the minimum latency in the control
group, while this component was most delayed among schizophrenics. Positive schizophrenia
symptoms correlated with the amplitudes of the left-hemisphere N170 component in response
to happy, fearful, and neutral faces. Our findings suggest that the facial expression deficit
in schizophrenia is related to delayed responses in face perception and is influenced by the
severity of positive symptoms. The evident delay in fearful face perception among patients
with schizophrenia may partly explain their inappropriate reactions to threatening conditions.
Keywords: emotional face perception, ERP, N170, schizophrenia, symptom severity.
1 Institute for Cognitive Science Studies (ICSS), Tehran, Iran.
2 School of Rehabilitation, Iran University of Medical Sciences (IUMS),
Tehran, Iran.
3 Department of Psychiatry, Tehran University of Medical Sciences (TUMS),
Tehran, Iran.
4 Department of Biomedical Engineering, Amirkabir University of Technology
(AUT), Tehran, Iran.
Correspondence should be addressed to M. Tehrani-Doost
(e-mail: tehranid@tums.ac.ir).
INTRODUCTION
Schizophrenia is a severe mental illness encompassing
a spectrum of cognitive, social, and emotional
impairments [1] and characterized by negative and
positive symptoms [2]. Despite compelling evidence on
deficient emotional face perception and recognition in
patients with schizophrenia, the processes underlying
these deficits are still open to debate [3]. Elucidating
the possible underlying causes for emotional face
processing disorder in schizophrenia would help
to suggest effective treatment interventions and
remediation strategies. The three main hypotheses
of this impairment are the following: (i) cognitive
impairment [4], (ii) early-stage visual processing
deficits [1], and (iii) general deficit in face or particular
emotional face processing [5, 6]. In terms of general
deficiency in facial recognition, some behavioral
studies indicated that patients with schizophrenia
suffer from an incapability of recognizing face identity
(i.e., age, sex, etc.) [7], distinguishing face familiarity
vs unfamiliarity [5], and/or providing face detection
[8]. A different approach has emphasized the role of
emotion-specific disorder in perception and recognition
of facial expressions [9]. According to Strauss et al.
[10], patients with schizophrenia have difficulties
in recognizing emotional faces during labeling or
matching tasks for different emotional faces. Schneider
et al. [11] reported that schizophrenia patients have
a weaker performance in emotional recognition
tasks even in easily recognizable emotions, like
happiness, without any deficit in age-discrimination
tasks, as compared to control subjects [11]. Various
neural networks are assumed to be involved during
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3280
M. AKBARFAHIMI, M. TEHRANI-DOOST, and F. GHASSEMI
processing of distinct facial emotions. For instance,
the amygdala has often been linked to fearful and
sad face processing, the cingulate sulcus and orbital
frontal cortical regions are shown to be activated by
viewing of happy and angry faces, respectively, and
the basal ganglia and insula are activated in response to
disgust faces [12]. Evidence from functional magnetic
resonance imaging (fMRI) studies has explained
some anatomical underpinnings of the deficits in
emotional face processing, such as hypoactivity
of the ventral temporal cortex, basal ganglia, and
prefrontal cortex [13], as well as hyperactivity of the
left hippocampal structures and right amygdala [14]
among schizophrenics. In addition, some behavioral
studies have substantiated deficits in recognizing
negative emotions during emotion identification and
discrimination tasks [6], while others emphasized the
impairment in recognizing particular emotional faces,
such as fearful [15], disgusted [5, 15], angry, and/or
sad [16].
Among the variety of methods used in face recog-
nition studies, recording of event-related potentials
(ERPs) is one of the most well-established techniques
currently applied to investigate the time course of neu-
ral responses to different facial expressions. The key
component in the face and facial expression studies
using ERPs is the N170 deflection [17, 18]. Recent
studies demonstrated that patients with schizophrenia
exhibit reduced N170 amplitudes during neutral and
emotional face processing [19-21]. Campanella et al.
[22] demonstrated the absence of “fear N170” modula-
tion in schizophrenia. On the other hand, while Bediou
et al. [23] recorded the decreased N170 amplitude in
the schizophrenia group during emotional face detec-
tion (fear, happiness, disgust, surprise, and neutral),
they did not report such a phenomenon during gender
detection tasks.
The specific contributions of schizophrenia sym-
ptoms to impairment in emotional face processing
are still controversial [24]. Some findings indicated
that patients with schizophrenia exhibit a cross-link
bet ween emotional faces but not age recognition
with regard to the severity of negative and positive
symptoms of the disease [7]. Meanwhile, some
researchers reported associations between positive
symptoms, age, and facial emotion recognition [25].
In contrast, van’t Wout et al. [26] found that, in the
“schizophrenia with fear deficits” group, negative
symptoms prevail. In the ERP studies, some authors
reported no relationship between the N170 parameters
and sub-scales of the Positive and Negative Syndrome
Scale (PANSS) [5, 27, 28], while others suggested
a strong association between the N170 indices and
negative symptoms using the “Scale for the Assessment
of Negative Symptoms” (SANS) global scores [29].
Despite extensive attempts to investigate the
impairment of facial expression recognition and
perception in schizophrenia, at present there are
limited ERP studies explaining the time course of each
emotional face perception. Very few such researches
examined the relationship between clinical symptoms
and facial expression perception. The main goals of
our study were: (i) to compare the amplitude and
latency of the N170 component between patients
with schizophrenia and matched healthy adults
while viewing emotional faces, and (ii) to examine
the relationship between the amplitude and latency
of N170 and the severity of positive and negative
symptoms in schizophrenia.
METHODS
Participants. Thirty patients suffering from
schizophrenia (16 man and 14 women) and 34 healthy
controls (19 men and 15 women) were enrolled in
the study. All control participants and schizophrenics
were right-handed (based on the Edinburgh inventory)
[30] and matched by age, sex, and their educational
levels. Diagnostic criteria for schizophrenia were
assessed through a semi-structured diagnostic
interview (Schedule for Schizophrenia and Affective
Disorder, SADS) [31] administered by a psychiatrist
and also through case-file reviews. Patients were
confirmed not to have other psychiatric co-morbidities
on DSM-IV-TR Axis I. Patients with schizophrenia
were recruited from the Roozbeh Psychiatry Hospital,
Tehran University of Medical Science (TUMS),
Tehran, Iran. Patients were enrolled during their stable
chronic phase of schizophrenia. Healthy participants
were free from any Axis I or Axis II disorders, history
of schizophrenia, or other psychiatric disorders in
their first-degree relatives. Across groups, the age
varied between 20 to 45 years, and the subjects had ≥ 9
years of formal education with normal or corrected-
to-normal visual acuity. Among the exclusion criteria,
there were a history of neurological disorders, loss
of consciousness due to a head injury, substance
dependence or history of substance abuse within the
preceding six months, a medical condition that might
affect cerebral functioning, and verbal IQ < 75.
Evaluation of Clinical Symptoms. Evaluation
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3 281
EMOTIONAL FACE PERCEPTION IN PATIENTS WITH SCHIZOPHRENIA
of psychopathological symptoms was performed
according to the PANSS. This instrument consists
of 30 clearly defined items. The PANSS entails
three subscales to assess positive (7 items), negative
(7 items), and general psychopathological (16 items)
symptoms [32].
Task and Original Stimuli. The participants
viewed all the stimuli presented on a 17-inch LG
monitor screen, in a dark and quiet room, while they
were comfortably seated on a chair with their head
positioned and fixed on a chin rest. The distance from
the monitor was 60 cm, with an approximately 8×11
deg visual angle. The experiment included one practice
and ten experimental blocks. Each experimental block
comprised presentations of five happy, sad, angry,
fearful, and neutral face images of Iranian validated
peoples. To maintain the vigilance throughout the task,
a house image (with a 10% probability of the total
number of stimuli) was used as the target stimulus.
The participants were instructed to press on the space
bar using their left index finger when responding to
the target stimuli.
All face images were in grayscale, oval-trimmed
(to remove background, clothing, and hairline),
and positioned within a rectangular frame (261 ×
365 pixel array). Each face was repeated 100 times
randomly. The pictures were viewed for 500 msec
and instantly replaced by a white fixation point in the
light gray background (1024 × 768 pixels) during the
1,000-msec-long interstimulus interval (ISI) with ±100
msec randomization. The stimuli were presented at the
middle of the monitor screen using Eevoke software.
Our aim was to comparatively assess the responses to
happy (positive facial expression), fearful (negative
facial expression), and neutral faces. This was done
through analyzing ERP records in response to the
above (happy, fearful, and neutral) facial stimuli.
EEG Recording. Continuous EEG signals were
recorded by 32 Ag/AgCl electrodes mounted in
an electrode cap (Waveguard, ANT, Netherlands)
according to the international 10-20 standard and
additional intermediate positions. Electrooculogram
(EOG) electrodes were placed on the outer canthus
of each eye, inferior and superior to the left orbit,
so as to monitor horizontal and vertical oculomotor
artifacts, respectively. Electrode impedances were
maintained below 5 kΩ. A 64-channel amplifier (ANT,
Netherlands) was used for data recording, and ASA
4.7.1 software was used for data acquisition. The
sampling rate was 512 sec–1. EEG was recorded online
with a 50-Hz notch filter.
ERP Extraction. EEG data were analyzed off-line
using ASA 4.7 (ANT, Netherlands), EEGLAB 9.0.8.6.b
(a freely available open source toolbox, http:// www.
sccn.ucsd.edu/eeglab) and MATLAB 7.10.0 (Math
works, USA) software. Raw data were filtered with
a band-pass filter of 1 to 80 Hz and referenced to
the mastoids average. Similar to our previous report
[33], the eye movement artifacts were canceled using
independent component analysis (ICA). A combination
of the efficient variant of fast ICA (EFICA) and efficient
weight-adjusted SOBI (EWASOBI) was chosen as the
ICA method using ICALAB software. In addition,
the remaining artifacts with deflection amplitudes of
±100 μV from the baseline were eliminated (primarily
through automatic artifact reduction by EEGLAB
9.0.8.6.b software and secondarily, through visual
inspection made by an expert). Artifact-free EEG
recordings were then segmented into epochs ranging
from 250 msec pre-stimulus to 1,000 msec post-
stimulus. Each channel baseline epoch was corrected
by prestimulus voltage subtraction.
Feature Extraction. The N170 component of visual
ERPs is a negative waveform peaking approximately
155-190 msec post-stimulus. It is mostly observed
in the occipito-temporal sites and, as is commonly
supposed, represents the earliest stage of facial
structure encoding [17, 19]. Our detection method for
this component was in line with earlier experiments.
The maximum-peak amplitude and latency values
were automatically extracted from occipito-temporal
records (P7, P8) [22, 34] within the time window of
130 to 250 msec, and all peaks were confirmed by
visual inspection.
Data Processing. Mean values of the amplitude and
latency were statistically analyzed using repeated-
measure analysis of variance (ANOVA) comprising
the following core factors: hemisphere (left and right),
facial expression (happy, fearful, and neutral), and
groups (patients and controls). Greenhouse-Geisser
correction was used for the degrees of freedom. In
addition, to calculate the direction and magnitude of
the association between N170 measures and clinical
features, we applied the Spearman’s rho nonparametric
correlation in SPSS 17.0. Throughout the experiment,
differences with P < 0.05 were considered significant.
RESULTS
Eight participants were excluded from the study.
These included four control subjects due to excessive
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3282
M. AKBARFAHIMI, M. TEHRANI-DOOST, and F. GHASSEMI
rejected trials, two patients due to inaccuracies in the
PANSS scores, and finally two other control subjects
in order to better maintain group matching by age and
sex. Altogether, 28 patients (16 men and 12 women)
and 28 control subjects (16 men and 12 women) were
included in the study (details are summarized in
Table 1).
The mean and s.e.m. values for the N170 amplitude
and latency in response to different facial expressions
are shown in Table 2. The grand averages of the N170
waveforms across the three types of facial expressions
(P7/P8) are illustrated in Fig. 1.
Repeated-measure ANOVA demonstrated a
significant main effect of the hemisphere (F [1, 54] =
= 40.83, P = 0.001) and the interaction effect of
hemisphere×facial expression (F [2, 108] = 5.43, P =
= 0.006) on the N170 amplitude. Pairwise comparisons
revealed larger N170 peaks throughout the right
hemisphere in both groups. No significant main effects
of facial expression and interaction effects of facial
expression×group, as well as hemisphere×group on the
N170 amplitude, were documented. Moreover, the two
groups showed no significant difference in terms of
the N170 amplitude.
With regards to the N170 latency, repeated-
measure ANOVA revealed a significant main effect of
the group (F [1, 54] = 4.25, P = 0.044). The result
of pairwise comparison indicated that the N170
latency tended to be shorter in the left hemisphere.
Moreover, for schizophrenics, further analysis of
TABLE 1. Characteristics of the Two Studied Groups (Schizophrenia Patients and Control Subjects)
Т а б л и ц я 1. Характеристики двох обстежених груп (пацієнтів із шизофренією та контрольних суб’єктів)
Characteristics Schizophrenia group
(n = 28)
Control group
(n = 28)
Intergroup difference
t P
Age (years) 33.32 ±5.65 32.61 ± 6.01 0.45 0.65
Education (classes, years) 12.57 ± 2.7 15.12 ± 3.20 –3.2 0.002
Illness duration (years) 11.5 ± 6.92
PANSS scores
Positive symptoms 21.27 ± 6.61
Negative symptoms 21.82 ± 6.98
General 42.79 ± 13.11
Footnote. Means ± s.d. values are shown.
F i g. 1. Grand-average of the
N170 components in ERPs
recorded from the left and right
hemispheres (P7/P8) in response
to presentations of happy (A),
fearful (B), and neutral (C) face
images among the schizophrenia
(1) and control (2) groups.
Р и с. 1. Усереднені в межах
груп компоненти N170,
відведені від лівої та правої
півкулі (P7/P8), в умовах
пред’явлення зображень облич
зі щасливим (A), переляканим
(B) і нейтральним (C) виразом у
групі пацієнтів із шизофренією
(1) та в контрольній групі (2).
μV
A
P7
P8
B C
μV μV
5
5
10
10
15
0
0
–5 N170
1
1
2
2
N170 N170
N170
msec
N170N170
–5
–10
–15
–250 –250 –2500 0 0250 250 250500 500 500750 750 750
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3 283
EMOTIONAL FACE PERCEPTION IN PATIENTS WITH SCHIZOPHRENIA
(F [2, 108] = 3.57, P = 0.039) on the N170 latency.
Despite the different intergroup trend of the N170
latency in response to different facial expressions
(Fig. 2) in terms of the time course and priority,
separate post-hoc analysis between different facial
expressions in each group showed no significant
difference for the N170 latency in response to faces
in both groups. Nevertheless, the N170 latency in
response to fearful faces was the only significantly
differing measure between the two groups (t = 2.95,
P = 0.005).
No relat ionships were found between the
N170 ampli tude/latency and negative/general
psychopathology symptoms in the schizophrenia
group. However, the positive symptoms demonstrated
a significant correlation with the “left” amplitude of
N170, as are shown boldfaced in Table 3.
DISCUSSION
The aims of our study were, firstly, to compare the
ERP features of the N170 component among patients
with schizophrenia and healthy controls when
passively viewing the posed happy, fearful, and
neutral face images and, secondly, to investigate the
relationship between the N170 characteristics and
clinical symptoms (using PANSS) of schizophrenia.
The study yielded three main results. First, in terms of
comparing the N170 between the two groups, patients
with schizophrenia exhibited longer latencies and
smaller N170 peaks in response to happy, fearful, and
neutral faces regardless of their expressions than those
in the control group. Moreover, the only significant
difference between the two groups was the disparity in
the N170 latency. What is inferred from this finding is
msec
190
185
180
2
1175
170
Happy Fearful Neutral
F i g. 2. Dependence of the mean values of the N170 latency, msec,
on the facial expression in the presented images; 1 and 2) control
group and patients with schizophrenia, respectively.
Р и с. 2. Залежність середніх величин латентного періоду
(мс) компонента N170 від виразу обличчя на пред’явлених
зображеннях у контрольній групі (1) та групі пацієнтів із
шизофренією (2).
TABLE 2. Parameters of Component N170 in Event-Related EEG Potentials Evoked in Response to Presentation of Images of Facial
Expression
Т а б л и ц я 2. Параметри компонента N170 у складі пов’язаних з подією потенціалів, котрі були викликані пред’явленням
зображень облич з різними виразами
Parameters Facial expression
Left hemisphere Right hemisphere
schizophrenia group control group schizophrenia group control group
Amplitude, mV
fearful –11.94 ± 2.15 –13.57 ± 1.55 –16.62 ± 2.45 –21.88 ± 2.6
happy –10.93 ± 2.04 –11.74 ± 1.62 –18.02 ± 2.08 –21.79 ± 2.7
neutral –11.14 ± 1.9 –10.89 ± 1.99 –18.18 ± 2.55 –22.39 ± 2.6
Lattency, msec
fearful 192.72 ± 5.33 170.93 ± 4.2 183.03 ± 3.74 176.38 ± 3.70
happy 186.5 ± 4.11 176.27 ± 4.3 180.10 ± 2.08 182.66 ± 3.91
neutral 186.44 ± 4.94 177.24 ± 4.09 183.24 ± 3.25 179.96 ± 3.48
Footnote. Means ± s.e.m. are shown.
hemisphere×group (F [1, 54] = 4.64, P = 0.036)
interaction suggested that, although the N170 response
to different facial expressions in this group is delayed
in both hemispheres (as compared to the controls),
this disparity between the two groups is particularly
significant in the left hemisphere (hemispheres: left,
t = –2.58, P = 0.013 vs right, t = –0.60, P = 0.545).
Repeated-measure ANOVA indicated the significant
interaction effect of facial expression×group
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3284
M. AKBARFAHIMI, M. TEHRANI-DOOST, and F. GHASSEMI
that, regardless of the particular expression, faces are
processed in almost the same way in the schizophrenia
group as in the control group; however, the perception
process is carried out later. This delay in the early stage
of perception may possibly lead to face recognition
deficits among patients with schizophrenia. To arrive
at a more solid conclusion with this respect, other
emotional faces and their related elicited components
should be investigated. This finding is consistent
with other reports in terms of N170 deficiencies in
schizophrenia. According to Campanella et al. [22],
subjects with schizophrenia tend to exhibit smaller
amplitudes of P100 and N170 with delayed latencies
when assigned to the emotional face oddball task
(neutral faces as frequent stimuli, and sad, fearful, or
happy faces as target stimuli). This has been linked
to deficiencies in the early stage of face perception
among these patients. Turetsky et al. [21] reported
significant group differences for the N170 component
features, which were sensitive to face structural
encoding but not to the affect modulation of the N250
component. The authors concluded that emotional
face recognition deficits are potentially due to faulty
structural encoding of faces in the patient group [21].
Along with these lines, Caharel et al. [5] reported the
smaller amplitudes and longer latencies of P1 and N170
in response to facial expressions (disgust, happy, and
neutral) and familiarity tasks. They proposed that this
deficit was possibly due to a generalized dysfunction
at sensory (P1) and perceptual (N170) stages of face
processing. Based on some other reports, when patients
with schizophrenia passively attend to emotional faces,
their N170 a features represent characteristically a
similar pattern. Lower amplitudes and prolonged
latencies of the N170 component, as compared to those
in normal subjects, were shown. However, the extent
of these dissimilarities varied in different studies [19,
27]. The findings vary among different investigations,
including ours. The inconsistency in the amplitude of
N170 in various reports may be due to the type of the
task [22] or of emotional faces [5, 21], and differences
in the signal analysis method (mean global field power,
while we examined the mean amplitude) [5, 27].
In contrast, several authors have reported the N170
components of almost the same features in response to
facial expressions in both groups. Wynn et al. [35] pro-
posed similar trends of P100 and N170 in the schizo-
phrenia and control groups in response to fearful,
angry, ashamed, happy, sad, and surprised faces. How-
ever, they found a significant difference in N250 (in
response to emotional faces) between the two groups.
The inconsistency seen between the above data and
that of ours may at least partly be due to the differ-
ence in time windows for N170 examination (140-220
TABLE 3. Correlations between the Amplitude and Latency of Component N170 and Clinical Symptoms in the Schizophrenia Group
(n = 28)
Т а б л и ц я 3. Кореляція між величинами амплітуди й латентного періоду компонента N170 і виразністю клінічних
симптомів у групі пацієнтів із шизофренією (n = 28)
N170 parameter/hemisphere
Facial expressions Positive symptoms Negative
symptoms
General psychopathology
symptoms
rho
Amplitude / Left fearful –0.57** 0.18 –0.02
happy –0.49** 0.02 –0.13
neutral –0.48** 0.13 –0.05
Latency / Left fearful –0.39* –0.15 –0.15
happy –0.28 –0.01 –0.01
neutral –0.29 –0.13 –0.13
Amplitude / Right fearful –0.14 0.005 0.005
happy 0.02 0.1 0.1
neutral –0.26 0.02 0.02
Latency / Right fearful 0.08 –0.08 –0.08
happy –0.05 –0.15 –0.15
neutral –0.26 –0.2 –0.20
Footnotes. rho) Spearman’s rank correlation coefficient. One and two asterisks show cases of significant correlations with P < 0.05 and
< 0.04, respectively. Positive symptoms demonstrating a significant correlation with the “left” amplitude and latency of component N170
are shown boldfaced.
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3 285
EMOTIONAL FACE PERCEPTION IN PATIENTS WITH SCHIZOPHRENIA
msec in other studies vs 130-250 msec in the current
investigation).
Second, our findings have demonstrated significant-
ly different trends for the N170 latency in response
to fearful, happy, and neutral faces between the two
groups. In our control group, regardless of the hemi-
sphere effect of facial expressions, the fastest N170
response was evoked to presentation of fearful faces
(followed by happy and neutral faces). Conversely, re-
sponses to fearful faces were the slowest in the schizo-
phrenia group, as compared to other facial expressions
(Fig. 2). Given the above, the emotional face percep-
tion in schizophrenia patients compared to controls
turned out to be not only more delayed but also hav-
ing different characteristic features. As expected, the
fearful expression (as a threatening stimulus), which
requires a faster response to danger, fear, and misery,
was related to the shortest-latency N170 in the nor-
mal group. In contrast, the schizophrenia group failed
to show such sensitivity to fearful stimuli. The above
finding is in line with those of Campanella et al. [22],
Lee et al. [27], and Kirihara et al. [36]. As was indi-
cated in some studies, the difference in emotional face
responses between the two groups is seen in the sub-
sequent components, mainly the N250 [35]. According
to Herrmann et al. and An et al. [28, 37], the emotional
face perception deficits in schizophrenia is predomi-
nantly due to the failure in the decoding phase and a
decrease in the positive amplitudes at 300 msec over
the parietal brain areas. We have not studied other ERP
components; however, we can expect that this dispar-
ity in early-stage face processing can potentially affect
the subsequent components, such as N250 or P300.
On the other hand, according to the study of Gur
et al. [38], the performance of schizophrenia-group
patients with the flat affect was poorer than that in
the healthy group, and this impairment corelated ex-
clusively with positive clinical symptoms. Although
the methodology and task type of the above study
is entirely different from those in our work, we may
atribute link longer latencies of N170 (modulated by
positive symptoms) to a blunted affect seen in schizo-
phrenia.
Third, considering our own results, the amplitude of
the left N170 in response to happy, fearful, and neutral
faces and also the latency of the left N170 in response
to fearful faces are modulated by positive symptoms
in patients with schizophrenia. In other words, regard-
less of the type of facial expressions, a greater sever-
ity of positive symptoms induces more engagement of
the neural processors during the face encoding (the
absolute value of the N170 amplitude). The relation-
ship between positive symptoms and the amplitude
of N170 is consistent with Campanella et al. [22] and
Turetsky et al. [21]; however, they found this relation-
ship with bilateral N170s. As opposed to Thoma et al.
[39] who found that the negative symptoms in patients
with schizophrenia correlated with the dysfunction of
right-hemisphere and sensory gating impairments, Hi-
gashima et al. [40] demonstrated an association be-
tween the left posterior temporal region with positive
symptoms presentations, such as delusions and thought
disorders [40]. As expected, the correlation between
abnormal activation of the left medial and lateral tem-
poral regions with positive symptoms may be one rea-
son for the modulation of the left N170 amplitude in
response to facial expression.
From a neuroimaging point of view, results of an
fMRI study in schizophrenia have demonstrated
the relationship between clinical symptoms and
impairments of some particular brain regions that are
typically involved during emotional tasks. Since the
correlation between positive symptoms and the activity
of the amygdala, hippocampal/parahippocampal
structures, and medial prefrontal cortex has been
established [2], it may be concluded that the
impairment of some key regions, such as amygdala
(which plays an important role in detection of
emotional and, especially, fearful faces) is influenced
by positive symptoms. Moreover, the severity of
positive symptoms may influence compensatory
mechanisms in brain circuits [41]. The need to further
explanation of these possible mechanisms makes
additional basic and complex facial expression studies
worthwhile.
Finally, the main limitations of our study should
be noted. Firstly, all participants in the patient group
were on medication that could not be changed because
of ethical reasons. So, we did not examine the effect
of medicine on the N170 component that can be
influenced by some types of drugs. Secondly, we did
not compare the facial perception in different types of
schizophrenia, and this was due to the limited sample
size.
To conclude, the impairment of “facial expression”
perception in schizophrenia is potentially linked to
delays in face perception per se, regardless of the
expressions. Interestingly, the amplitude of the left-
hemisphere N170 in response to happy, fearful, and
neutral faces and the latency of the N170 evoked
by fearful faces were influenced by the severity of
positive symptoms in schizophrenia. The delay in
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 3286
M. AKBARFAHIMI, M. TEHRANI-DOOST, and F. GHASSEMI
perception of fearful faces in schizophrenia can be
considered as one of the many reasons explaining
inappropriate reactions of these patients to threatening
conditions.
The ethical protocol of this study was based on the Helsinki
Declaration, and written informed consent signed by all
participants prior to their enrollment was obtained.
Acknowledgment. This study was a part of the first author’s
thesis to obtain the PhD degree in cognitive neuroscience (brain
and cognition) at the Institute for Cognitive Science Studies,
Tehran, Iran.
М. Акбарфахімі1,2, М. Техрані-Доост3,1, Ф. Гассемі4,1
СПРИЙНЯТТЯ ЕМОЦІЙНОГО ВИРАЗУ ОБЛИЧЧЯ У
ПАЦІЄНТІВ, КОТРІ СТРАЖДАЮТЬ НА ШИЗОФРЕНІЮ:
ДОСЛІДЖЕННЯ З ВІДВЕДЕННЯМ ПОВ’ЯЗАНИХ З
ПОДІЄЮ ЕЕГ-ПОТЕНЦІАЛІВ
1 Інститут з дослідження когнітивних функцій (ICSS), Теге-
ран (Іран).
2 Інститут реабілітації, Ірінський медичний університет,
Тегеран (Іран).
3 Тегеранський медичний університет, Тегеран (Іран).
4 Технологічний університет, Аміркабір (АІІ), Тегеран
(Іран).
Р е з ю м е
У пацієнтів, котрі страждають на шизофренію, розпізнаван-
ня виразів обличчя є серйозно порушеним. Оскільки проце-
си, що зумовлюють подібний дефіцит, вивчені недостатньо,
ми намагалися дослідити співвідношення сприйняття вира-
зів обличчя та клінічних симптомів у пацієнтів із цим за-
хворюванням. В обстежувану групу ввійшли 28 пацієнтів із
діагнозом шизофренія та 28 дорослих суб’єктів; групи були
узгоджені в статевому та віковому аспектах. У представни-
ків цих двох груп вимірювали та порівнювали амплітуду
й латентний період компонента N170 у складі пов’язаних з
подією потенціалів, викликаних пред’явленням зображень
облич зі щасливим, переляканим і нейтральним виразом.
Потім оцінювали взаємозв’язок параметрів N170 з оцінка-
ми клінічних симптомів шизофренії згідно зі шкалою пози-
тивних і негативних синдромів (PANSS). Розвиток компо-
нента N170 після пред’явлення зображень облич з різними
виразами відбувався у пацієнтів із шизофренією істотно
пізніше, ніж у здорових контрольних суб’єктів [F (1, 54) =
= 4.25, P = 0.044]. N170 після пред’явлення переляканих об-
лич (порівняно зі щасливими та нейтральними) розвивався
у суб’єктів контрольної групи з мінімальною затримкою, а
у шизофреників він виникав значно пізніше. Інтенсивність
позитивних симптомів у шизофреників корелювала з амп-
літудами N170 у лівій півкулі після пред’явлення як щас-
ливих, так і переляканих і нейтральних облич. Наші спо-
стереження показують, що дефектність сприйняття виразу
обличчя у пацієнтів, хворих на шизофренію, пов’язана із
затримкою відповідей ЦНС, і на таку дефектність впливає
тяжкість позитивних симптомів. Очевидна затримка сприй-
няття облич з переляканим виразом у пацієнтів із шизофре-
нією може частково пояснювати неадекватність їх реакцій
на загрозливі ситуації.
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