Facial emotion perception in young female students with subsyndromal panic disorder. Behavioral and ERP study
Introduction
Today’s world with its stream of negative information and stressing factors creates strong prerequisites for anxiety disorders, in particular, panic disorder (PD). Patients with PD are extremely sensitive to dangerous environmental signals and are highly vulnerable to unexpected anxiety events, which is key in maintenance of the disease (Bar-Haim et al., 2007; Fonzo et al., 2015; Killgore et al., 2014; Pauli et al., 2005; Windmann et al., 2002). Together with full-blown PD, subthreshold, or subsyndromal forms of panic disturbances have become common, and some people experience clinically relevant panic symptoms without meeting the diagnostic criteria for PD (Batelaan et al., 2007a, 2007b; Ophuis et al., 2018).
Epidemiological studies have shown that subthreshold mental illnesses, especially in the realm of affective disorders occur across all age groups and are between two and four times more common than illnesses with specific diagnoses (Helmchen and Linden, 2000). According to Batelaan et al. (2006), the life time prevalence of panic disorder is 2.1 %, while subsyndromal panic disorder is more prevalent (limited symptom attacks 7.5 %, infrequent panic attacks 5.1 %). Many authors emphasize that individuals with subthreshold forms of mental disorders suffer from a similar impact on their quality of life and functioning as individuals with full-blown illnesses (Batelaan et al., 2007a, 2007b; Magruder and Calderone, 2000; Ophuis et al., 2018). In psychiatric research, diagnostic criteria set more or less artificial cutoff scores for the presence of a disorder. However, when group comparisons between patients and healthy controls are conducted, individuals that don’t meet the diagnostic criteria but show some clinical symptoms are usually excluded. Study of individuals with subthreshold forms of psychopathology will help to better understand the nature of the neural mechanisms underlying psychiatric disorders.
Unfortunately, thus far, biological research in patients with subthreshold or subsyndromal forms of mental disorders remain limited (Besteher et al., 2017; Gottesman and Gould, 2003; Laeger et al., 2012; Woody and Gibb, 2015). These studies are primarily focused on neural correlates of emotion processing in subjects with high trait anxiety as a stable personality factor or with subclinical depressive symptoms. For example, impaired neural processing of facial expression has been found in healthy individuals with heightened trait anxiety (Eldar et al., 2010; Holmes et al., 2009; Rossignol et al., 2005; 2012) or in subjects with high anxiety sensitivity (Poletti et al., 2015; Taake et al., 2009). Several studies have observed a positive correlation between anxiety measures and the activation of the amygdala during emotional face processing (Etkin et al., 2004; Sehlmeyer et al., 2011), as well as negative word reading (Laeger et al., 2012).
The pathophysiology of PD still remains to be elucidated. Functional neuroimaging studies have shown findings concerning the comprehension of neural substrates related to PD (Chechko et al., 2009; de Carvalho et al., 2010; Goddard, 2017; Gorman et al., 2000; Lai, 2019). The core concept for pathophysiology in PD is the fear network model (FNM) (Gorman et al., 2000). The center of the traditional FNM is the amygdala, which is connected with the medial frontal cortex and hippocampus for the control of fear response and fear memory. In addition, the projections from the amygdala are linked with the brainstem and hypothalamus for panic symptoms related to dysfunction of the autonomic nervous system. However, more extended areas of the FNM have been discovered in recent imaging studies, including the sensory regions of the occipital cortex, parietal cortex, temporal cortex, and insula (Lai, 2019).
Many authors have described the behavioral (Lissek et al., 2010; Reinecke et al., 2011; Wang et al., 2013) and neurophysiological correlates of an attentional bias toward threat-related facial stimuli in patients with PD (Chechko et al., 2009; Pauli et al., 2005; Shim et al., 2016; Stevens et al., 2018; Windmann et al., 2002). A systematic review of evoked potential studies in PD linked the diagnosis to impairments in attention, information processing, and responsiveness to new stimuli (Di Giorgio et al., 2015). A large number of studies give evidence that patients with PD demonstrate altered emotion recognition in particular, they tend to show excessive ERPs to threatening stimuli (Cai et al., 2012; Dymond et al., 2015; Kessler et al., 2007; Lissek et al., 2010; Wang et al., 2013). This attentional bias towards information related to physical or social threat seems to be more frequently discussed as a correlate of panic disorder (Dymond et al., 2015; Lissek et al., 2010). It was observed that symptom severity of PD might be associated with impairment in emotion processing of threat-related facial expressions (Wang et al., 2013). This characteristic was not dependent on whether the patients were medicated or not, nor the type of task performed (Chechko et al., 2009; Reinecke et al., 2011). For example, untreated patients with PD showed similar exaggerated attentional biases to negative faces as well as negative word stimuli in different experimental paradigms, specifically, the Facial Expression Recognition task, a Faces Dot Probe task, and an Emotional Stroop task (Reinecke et al., 2011). One may suggest that this attentional bias is an inherent feature of panic disorder and it can be observed even at the subsyndromal stage of the disorder.
In the present study, we investigated behavioral characteristics and cortical visual event-related potentials (ERPs) during the task of recognizing different emotional expressions in photographs of faces performed by young female students with subsyndromal panic disorder (SPD) in comparison with matched healthy controls. These women experienced infrequent panic attacks only during emotional stress during examination sessions; they had not previously visited doctors, were non-medicated, and were identified only when interviewing a large population of students.
Section snippets
Subjects
Thirty two young female students were recruited from the Pirogov Russian National Research Medical University, Moscow, Russia. All had normal or corrected-to-normal vision. Inclusion criteria were right-handedness and no current or former severe neurological or psychiatric disorder. Fifteen young female students (mean age 19.9 ± 0.5 years) were included in the subsyndromal panic disorder (SPD) group. Clinical interviews were conducted by S. Gordeev based on the Structured Clinical Interview for
Anxiety scores
The participants with SPD differed from the healthy controls, with higher trait anxiety scores (55.15 ± 3.89 vs 41.13 ± 2.12; T = 3.98, df = 30, p = .003). Between-group differences in state anxiety scores were not found (36.91 ± 4.56 vs 36.00 ± 2.38; T= 0.96, df=30, p=0.95).
Behavioral data
Fig. 2 shows the response time and accuracy means and standard errors for four emotional expressions in the healthy and SPD groups.
Response time was significantly affected by Emotion, F(3,75) = 11.66, p < .001, ε = .68, ηp2
Discussion
In the present study, we compared behavioral and ERPs correlates of facial expression recognition in a nonclinical sample of young women with subsyndromal panic disorder (SPD) and in healthy controls, which were matched by sex, age, and education level (all subjects were 2nd-year students of Pirogov Russian National Research Medical University, Moscow). The participants with SPD experienced rare panic attacks that occurred mainly due to situations of emotional stress (e.g., during exam
Conclusion
We compared behavioral and neural correlates of facial emotion recognition in non-medicated young women with SPD and matched healthy controls. The SPD subjects did not differ from healthy controls in the behavioral characteristics, but they showed a slower response to fearful expression compared to neutral and happy expressions. However, SPD subjects had altered ERP characteristics of facial expression recognition. These were manifested in an increased occipital P100 amplitude, a greater P200
Limitations
There are several limitations associated with the present study. The first limitation is the relatively small number of subjects with SPD that were included. This may be the reason for the failure to find significant interactions between emotion and group. However, the overall pattern of results suggests that in SPD subjects but not in healthy controls, attention is biased in favor of threatening facial expressions. Further studies involving larger samples are needed.
Despite the small size of
Article Information
From the Institute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences (VK, ES, NG, AK), and Pirogov Russian National Research Medical University (SG), Moscow, Russia. EM conceived of the study and participated in its design. VK took part in data collection and wrote the manuscript. NG participated in study design. SG made the diagnoses of SPD by interviewing patients with panic attacks. EM, VK, AK, and NG participated in data analysis and manuscript discussion.
Declaration of Competing Interest
The authors report no biomedical financial interests or potential conflicts of interest and have agreed to publish this manuscript.
Acknowledgments and Disclosures
The study was supported by the Russian Foundation for Basic Research grant No. 16-06-00945-OGN, «Factors of psychosocial disadaptation in persons with various forms of psychovegetative disorders», and funds within the state assignment of the Ministry of Education and Science of the Russian Federation. Electrophysiological studies were carried out using equipment of the Research Resource Center of IHNA and NPh RAS for functional brain mapping.
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