Neuropsychological test performance in social anxiety disorder MIA SKYTTE O’TOOLE, ANDERS DEGN PEDERSEN, ESBEN HOUGAARD, NICOLE K. ROSENBERG,

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O’Toole MS, Pedersen AD, Hougaard E, Rosenberg NK. Neuropsychological test performance in social anxiety disorder. Nord J Psychiatry 2015;69:444–452. Background: The effect of state factors on neuropsychological performance in social anxiety disorder (SAD) has not been thoroughly investigated and the overall neuropsychological profile remains poorly understood. Aims: The primary objective of the study was to investigate the effect of state anxiety and state emotion suppression on neuropsychological performance in SAD. Methods: A neuropsychological test battery was administered before and after an anxiety manipulation (instruction to give a video-recorded speech) to 42 patients with SAD and to a gender and education matched group of 42 healthy controls (HCs). Results: Overall, participants with SAD performed worse than HCs on processing speed, visuospatial construction, visuospatial memory, verbal learning and word fluency, of which only the decreased visuospatial construction performance was considered clinically significant. State anxiety was not associated with neuropsychological performance at baseline, whereas state emotion suppression predicted decreased visuospatial memory in HCs and decreased verbal learning in the SAD group. Both groups performed better on working memory, processing speed and spatial anticipation, and worse on verbal learning and memory following the anxiety manipulation. The increase in state anxiety was associated with the decrease in verbal learning in both groups. Conclusions: Participants with SAD showed clinically significant difficulties with visuospatial construction and may experience verbal learning difficulties when suppressing emotions and experiencing an increase in anxiety. • Cognitive functioning, Emotion regulation, Emotion suppression, Neuropsychology, Social phobia. Mia Skytte O’Toole, Department of Psychology and Behavioral Sciences, School of Business and Social Sciences, Aarhus University, Bartholins Allé 9, 8000 Aarhus C, Denmark, E-mail: [email protected]; Accepted 8 December 2014.

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ocial anxiety disorder (SAD) is a disabling disorder characterized by a persistent fear in or avoidance of social situations (1). There are many negative outcomes associated with the disorder, among which are low academic performance and poor quality of life (2, 3). Relatively many patients with SAD do not seem to benefit from available evidence-based treatments such as cognitive–behavioral therapy (4). While a non-response to treatment could be due to a variety of factors, neuropsychological impairments could indeed play a crucial role. For instance, poor executive functioning, such as poor organizational skills, may hinder the planning and execution of homework assignments. Furthermore, SAD has been associated with a number of cognitive biases (5) that all play an important role in cognitive models of SAD. These models assume that individuals with SAD are biased in their processing of socially ambiguous

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information (e.g. 6, 7). However, it would be important to investigate if such biases could be due to neuropsychological deficits. The neuropsychological profile of SAD has not been thoroughly investigated and therefore remains poorly understood. Prior to this study, a systematic review of neuropsychological performance in SAD was conducted (8). The review included 30 studies, of which only six primarily focused on neuropsychological performance in SAD. The remaining 24 studies mainly investigated cognitive biases but included neuropsychological tests. The review revealed that individuals with SAD consistently showed decreased performance on tests of visuospatial and constructive ability, and there was some indication of decreased performance on tests of verbal memory functions. Since the systemic review was conducted, Sutterby & Bedwell (9) has compared individuals with

DOI: 10.3109/08039488.2014.997288

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SAD with a group of controls on a variety of neuropsychological tests and reported no between-group differences. In accordance with the review, individuals with SAD did perform worse than controls on visual working memory (Cohen’s d ⫽ 0.6), however, this finding disappeared after the authors adjusted the P-value. In the above referenced review, some support was found for depression to be associated with decreased neuropsychological test performance. The severity of trait social anxiety was also explored in the review, but it showed no associations with neuropsychological performance. The influence of state factors on neuropsychological functioning remains poorly investigated. Two state factors are of focus in this paper: state anxiety and state emotion suppression. Regarding state anxiety, one may suspect individuals with SAD to experience more anxiety in a test situation as he or she is being exposed to a typical SAD-related fear, namely that of being evaluated by another person. An increased state anxiety level may lower neuropsychological test performance. For instance, individuals under the influence of stress have been shown to take longer time to complete spatial working memory tasks (10). Furthermore, the direct manipulation of stress hormones has been associated with decreased attention, concentration and mental speed (11). In addition, the association between anxiety/stress and neuropsychological performance may be curvilinear as described in the classic Yerkes & Dodson (12) law of the U-shaped association between arousal and cognitive performance. Several experiments have confirmed that there is a positive relationship between cognitive performance and arousal up to a certain point, after which higher levels of arousal have a negative influence on the performance (13). Test anxiety among individuals with SAD could be assumed to easily exceed this point, partly due to their interpersonal sensitivity and partly due to their emotional hyperreactivity (e.g. 14). The very few studies on the influence of state anxiety on neuropsychological performance in SAD have revealed mixed results. One study found a negative association (15), while another found no association (16). Graver & White (17) directly manipulated the anxiety levels (by a speech task) and found group-specific effects. While healthy controls (HCs) generally performed better after the anxiety induction, participants with SAD either did not improve or performed worse. These results indicate that neuropsychological test performance could be influenced by both trait and state anxiety. Emotion suppression is another state factor that may be hypothesized to influence neuropsychological performance among individuals with SAD. Following Dunn and colleagues (18), emotion suppression in this paper refers to both the suppression of emotional expressions and the suppression or avoidance of inner feelings, the latter termed experiential avoidance by Hayes (19). Dunn NORD J PSYCHIATRY·VOL 69 NO 6·2015

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and colleagues (18) have argued that the regulation of emotional expressions is inseparable from the regulation of inner emotions. In non-clinical populations, expressive suppression has been found to be associated with poorer visual and verbal memory for emotional material (20– 22). Another study has shown that instructions to suppress both emotional expressions and internal sensations resulted in poorer recall of details from a distressing video (18). Emotion suppression is widely used by individuals with SAD (23, 24), but the effect of emotion suppression on neuropsychological performance in individuals with SAD has, however, not yet been studied. The lack of studies exploring the effect of state factors on neuropsychological performance is crucial, as the influence of state factors on neuropsychological performance needs to be considered in order to decide if any detected neuropsychological difficulties are to be considered stable, trait-like deficits, or rather situational difficulties influenced by state factors. The present study compared neuropsychological test performance in participants with SAD and HCs before and after an experimental anxiety manipulation (instruction to give a video-recorded speech). The aims of the study were twofold: first, to investigate neuropsychological test performance among participants with SAD compared with HCs by means of a fairly comprehensive neuropsychological test battery, and secondly, to explore the influence of state anxiety and state emotion suppression on neuropsychological test performance in SAD. Based on prior studies (8), it was hypothesized that participants with SAD would show poorer visuoconstructive ability, as well as poorer verbal learning and memory compared with HCs. Following the anxiety manipulation, participants with SAD, but not HCs, were expected to show decreased neuropsychological test performance, i.e. an interaction between time and group was expected. Both state (anxiety and emotion suppression) and clinical/trait factors (depressive symptoms, symptoms of social anxiety and use of psychotropic medicine) were explored in relation to between-group differences.

Methods Participants Participants with SAD were recruited from an outpatient anxiety clinic at Aarhus University Hospital, Denmark. Anxiety disorders were diagnosed according to DSM-IV criteria with the Anxiety Disorders Interview Schedule (ADIS-IV; 25), and other diagnoses were provided from clinical interviews based on ICD-10 criteria (the standard diagnostic system in Denmark; 26). All diagnostic interviews were conducted by a team of five clinicians, all familiar with the ADIS-IV, who met on a weekly basis to peer supervise diagnoses. Inclusion criteria were a primary diagnosis of SAD, Danish as primary language and

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age ⱖ 18 years. Exclusion criteria were a severe mental illness, including severe depression, and alcohol/drug abuse or dependency. All patients fulfilling the inclusion criteria were consecutively invited to participate. From January 2010 through August 2011, 94 patients with SAD were invited to participate in the study, and 42 were included (45%). The remaining patients either indicated that they did not want to participate (n ⫽ 30), failed to show up (n ⫽ 13) or were unable to schedule an appointment (n ⫽ 9). The patients who did not participate were slightly older (mean ⫽ 33.2) than the participants (mean ⫽ 29.2), t(86.9) ⫽ 2.02, P ⬍ 0.05, but did not differ on gender, χ2(1) ⫽ 0.004, P ⬎ 0.05, level of social anxiety, t(62) ⫽ 1.78, P ⬎ 0.05, or level of depression, t(57) ⫽ 0.12, P ⬎ 0.05. All participants with SAD had generalized SAD. Ten had one or more comorbid anxiety diagnoses (panic disorder with agoraphobia: n ⫽ 2, generalized anxiety disorder: n ⫽ 3, obsessive–compulsive disorder: n ⫽ 2, specific phobia: n ⫽ 2, chronic adjustment disorder: n ⫽ 1), 10 had a current depressive episode (single depressive episode: n ⫽ 3, recurrent major depressive episode: n ⫽ 7) and three had a dysthymic disorder. Twenty-six participants with SAD received psychopharmacological treatment (selective serotonin reuptake inhibitors [SSRI]: n ⫽ 17, serotonin–norepinephrine reuptake inhibitors [SNRI]: n ⫽ 6, anti-epileptics [pregabaline]: n ⫽ 4, tricyclic antidepressants: n ⫽ 2, norepinephrine and specific serotonergic antidepressants: n ⫽ 1). In order to match participants on different levels of education, HCs were recruited from various educational institutions (students seeking to get their general educational degree, students from different vocational schools and newly admitted college students). The students were informed about the project and invited to sign up as volunteers. From those willing to participate, the closest individual matches to SAD participants were chosen based on gender and level of education. Due to the recruitment of HCs from student populations, it was not possible to match groups on age. HCs were screened for psychiatric disorders with the same instruments as the participants with SAD. The diagnostic assessments were conducted by the first author under the supervision of the third author, a senior clinical psychologist with formal training in psychiatric diagnostics. Inclusion criteria were Danish as primary language and age ⱖ 18 years. Individuals were excluded if they had any current or prior psychiatric disorder, except for a single depressive episode that ended more than 6 months prior to inclusion. Twenty-two individuals were excluded; 19 due to the presence of a psychiatric disorder, and three due to insufficient Danish language proficiency. Demographic and clinical characteristics of the participants are shown in Table 1. There were no differences

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Table 1. Demographic and clinical characteristics of participants. SAD (n ⫽ 42), mean (s) Gender, % women Years of education Age Symptoms of social anxiety (LSAS) Depressive symptoms (BDI–II)

64 14.0 (2.1) 29.2 (7.9) 85.4 (28.6) 19.8 (13.1)

HC (n ⫽ 42), mean (s) 64 14.3 (2.2) 25.4 (6.6)* 22.3 (13.2)*** 3.3 (5.0)***

*P ⬍ 0.05, ***P ⬍ 0.001. s, standard deviation; HC, healthy control; SAD, social anxiety disorder; LSAS, Liebowitz Social Anxiety Scale; BDI–II, Beck Depression Inventory, second edition.

on the matching variables, gender or years of education, but participants with SAD were somewhat older than the HCs (mean difference ⫽ 3.8 years). Participants with SAD were also more socially anxious and more depressed.

Neuropsychological measures The neuropsychological test battery covered a broad spectrum of cognitive functions. The specific tests were chosen based on both their usage in previous studies (8) and their sensitivity to detect cognitive dysfunctions (27). General cognitive ability/intelligence: The Vocabulary and Matrix Reasoning Test from the Wechsler Adult Intelligence Scale—Third Edition (WAIS-III: 28). Working memory: The WAIS-III Digit Span and Letter-Number Sequencing Tests (28). Processing speed: The WAIS-III Digit-Symbol Coding Test (28). Verbal learning and memory: Rey Auditory Verbal Learning Test (RAVLT) (29, 30). The words from the word recognition task were used as an alternative version. Visuospatial construction and memory: Rey Complex Figure Test (RCFT) (30). Executive functioning: The Brixton Spatial Anticipation Test (BSAT) (31), in both an original and an alternative version. Phonological and categorical verbal fluency (revised from (32)) in two different versions: 1) F-words and “things you can see on the street” and 2) N-words and “animals”.

Psychological assessment STATE MEASURES State anxiety was measured on a visually presented scale from 1 to 10 (from no anxiety to the highest imaginable level of anxiety). We chose this simple one-item measure as state anxiety was repeatedly measured throughout the testing. Emotion suppression was measured by seven items that were rated on a 7-point scale. Three items concerned expressive suppression and were from the Emotion NORD J PSYCHIATRY·VOL 69 NO 6·2015

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Regulation Questionnaire (33), leaving out the item about suppression of positive emotions. Internal suppression was assessed by the four items from the Acceptance and Action Questionnaire (34) with the highest factor loadings onto experiential avoidance (35). Following Kashdan & Steger (36), the seven items were modified from a general statement to a statement targeting emotion suppression during the cognitive tasks, e.g. “During the cognitive tasks … I kept my emotions to myself ”. In accordance with Dunn and colleagues’ (18) suggestion of a close relationship between expressive and experiential suppression, an exploratory principal component analysis of the seven emotion suppression items produced only one factor, with loadings for all items ⬎ 0.64. The scale was therefore analyzed as a measure of a single construct: emotion suppression. The seven items indicated good reliability both times they were administered (Cronbach’s α ⫽ 0.90/0.92). TRAIT MEASURES Social anxiety was assessed by the self-report version of the Liebowitz Social Anxiety Scale (LSAS; 37), which consists of 24 items concerning general fear and avoidance of specific social situations (Cronbach’s α ⫽ 0.98 in this study). Depressive symptoms were measured with the Beck Depression Inventory, second edition (BDI-II), which is a 21-item self-report instrument concerning depressive symptoms within the past 2 weeks (38) (Cronbach’s α ⫽ 0.96 in this study).

Procedure The neuropsychological test battery was administered twice, before and after an experimental anxiety manipulation that was inspired by the well-validated Trier Social Stress Test (39). After the first neuropsychological assessment, the participants were informed that some of the tests had to be administered twice, in order to be certain of the results, and that they had to give a speech afterwards in front of a video-camera. A camera was then revealed and remained visible for the rest of the experiment. Participants were told that the speech should last 3 min, concern their latest out of town trip or vacation, and that their performance would later be evaluated by the first author and a research assistant (the speech procedure was carried out as a part of another study). Altogether, it took an average of 1½ h to complete the two test administrations. The WAIS-III tests for general cognitive abilities (Vocabulary and Matrix Reasoning) were only administered at baseline. The other neuropsychological tests were administered twice, before and after the anxiety manipulation, except for the RCFT construction trial, which cannot meaningfully be repeated. Alternative versions of the tests were given for the RAVLT, the BSAT and word fluency, while the same versions of the tests were used NORD J PSYCHIATRY·VOL 69 NO 6·2015

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for the working memory and processing speed tasks, since a practice effect was considered less likely here (cf. 17). The short delay memory task of the RCFT was used before the anxiety manipulation; the long delay memory task after. The order in which different versions of the tests were administered was quasi-randomized based on even vs. uneven numbered birthdays. State anxiety was measured before each cognitive task, i.e. 12 times before and nine times after the anxiety manipulation (the difference in measuring points reflects the difference in number of tests). State emotion suppression was assessed twice, immediately after the two administrations of the neuropsychological test battery. We only assessed emotion suppression twice, as repeated administrations of the whole scale would be inconvenient, and we expected the level of emotion suppression to be rather constant during the respective test administrations. All participants were given the trait questionnaires, BDI-II and LSAS, after they had finished the experiment, to be filled out at the clinic or returned by mail in a stamped and addressed envelope. The first author administered the experiment and the data collection. To ensure that the anxiety manipulation was conducted in the same way for all participants, it was read aloud from a manuscript. The neuropsychological testing was supervised by the second author, a licensed specialist in neuropsychological assessment. Participants were debriefed after the experiment. All participants were orally informed and provided written material about the study, and they signed written consent forms. Participants were not compensated for participation. The study was approved by the Local County Ethical Committee and by the Danish Data Protection Agency.

Analytic strategy The difference between the two versions of the neuropsychological tests (RAVLT, BSAP and word fluency) was investigated at baseline, comparing individuals with even and uneven numbered birthdays receiving the two versions in different order. Version type was included as a categorical covariate in subsequent analyses if a difference was found. Between-group differences on the neuropsychological variables that were only measured once (vocabulary, matrices and the copy task in RCFT), were evaluated with independent t-tests. The other neuropsychological performances were evaluated with mixed Time (before vs. after the anxiety manipulation)⫻ Group (SAD vs. HCs) analyses of variance (ANOVAs), controlling for test version type when appropriate. When a between-group difference was detected, Pearson correlation analyses were conducted between the neuropsychological variables and the state variables, separately for the two groups. Because the two groups differed on age, Pearson correla-

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tion analyses were also conducted between age and the neuropsychological measures. When a time effect was detected, the magnitude of change on the neuropsychological measures was correlated with the change on the state measures. For the SAD group, correlations were also calculated for the association between the neuropsychological variables, on which there was an overall between-group difference, and clinical variables. All between-group effect sizes were calculated into and expressed as Cohen’s d, i.e. all partial eta-squared effect sizes were converted into d-scores (40) for the ease of interpretation and comparison between different analyses. A d-value of 0.2, 0.5 and 0.8 were considered a small, medium and large effect size, respectively. Mean substitution was chosen as the method to handle single missing items on the BDI-II and LSAS, and was performed for each scale separately based on the individual’s mean. If a case had more than 50% missing data on the scale, no mean substitution was performed (cf. 41). Eleven (13%) and 16 individuals (19%) did not return in the BDI-II and LSAS, respectively. Two individuals had one or two missing items on the BDI-II, and six individuals had one or two missing items on the LSAS. One individual did not fill out the state emotion suppression measures. Two individuals had one missing state anxiety observation in which cases the last observation was carried forward.

Results Version type differences No differences were detected between the original (mean ⫽ 58.5) and the alternative (mean ⫽ 56.3) version on the RAVLT learning task, t(82) ⫽ 1.1, P ⫽ 0.272, d ⫽ 0.24, the original (mean ⫽ 12.1) and the alternative (mean ⫽ 11.5) version on the RAVLT retention task, t(82) ⫽ 1.2, P ⫽ 0.230, d ⫽ 0.27, or the “F-words and things you see on the street” version (mean ⫽ 32.9) and “N-words and animals” version (mean ⫽ 34.4), t(82) ⫽ ⫺ 0.8, P ⫽ 0.420, d ⫽ ⫺ 0.18. There was a difference on the BSAT between the original (mean ⫽ 11.0) and the alternative (mean ⫽ 7.7) version, t(77.6) ⫽ 3.7, P ⬍ 0.001, d ⫽ 0.84, and version type was therefore included as a covariate in analyses with the BSAT as the dependent variable.

Neuropsychological performance Raw neuropsychological test scores are presented in Table 2. Overall, between-group effects showed that the SAD group performed worse in five areas: processing speed; visuospatial construction accuracy; visuospatial memory; verbal learning and executive functioning (only word fluency). The association between age and performance in the five areas (before the anxiety manipulation)

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was explored. Age was positively correlated with word fluency performance, r ⫽ 0.26, P ⫽ 0.016; meaning that a higher age was associated with better performance on the test. As the association between state anxiety and cognitive performance has been described as a U-shape association, this association was visually inspected but a linear association seemed to best fit the data. Pearson correlations can be found in Table 3. Regarding state factors, state anxiety was not significantly correlated with neuropsychological performance, but was trend-wise associated with processing speed in the HCs and with visuospatial memory performance in the SAD group. State emotion suppression was negatively correlated with visuospatial memory performance in the HCs, and negatively correlated with verbal learning in the SAD group. It was also associated with processing speed and verbal learning performance in the HCs at the trend-level. Regarding the clinical variables, depressive symptoms and the use of medication were negatively correlated with verbal learning performance in the SAD group, as was symptoms of social anxiety at the trend-level.

Manipulation check and state factors Table 2 reveals the average scores for state anxiety and state emotion suppression. To check whether the anxiety manipulation was successful, a mixed ANOVA with Time (immediately before vs. after the manipulation) and Group (SAD vs. HC) was conducted. The anxiety level immediately before vs. after the manipulation was used, as an average measure would hold both the rise in anxiety but also a possible decrease after an initial scare of the upcoming speech task. The analysis showed that, overall, the SAD group was significantly more anxious, F(1, 82) ⫽ 67.3, P ⬍ 0.001, d ⫽ 1.8. A significant effect of Time was revealed, F(1, 82) ⫽ 40.2, P ⬍ 0.001, d ⫽ 1.4, i.e. the anxiety increased after the manipulation, and post hoc tests showed that the increase was significant in both the SAD (Δ ⫽ 1.6, standard deviation, s ⫽ 2.0, p ⬍ 0.001) and HC (Δ ⫽ 0.6, s ⫽ 1.1, P ⫽ 0.002) group. An interaction effect, F(1, 82) ⫽ 9.4, P ⫽ 0.003, d ⫽ 0.7, furthermore showed that the increase was largest for the participants with SAD. Regarding emotion suppression, the SAD group was overall engaging in more emotion suppression, F(1, 81) ⫽ 87.4, P ⬍ 0.001, d ⫽ 2.1, but there was no effect of Time, F(1, 81) ⫽ 0.01, P ⫽ 0.897, d ⬍ 0.1, and no interaction was revealed.

Effects of time and interaction effects The effect of Time was positive for working memory, processing speed and executive functioning (only BSAT), whereas it was negative for verbal learning and memory. The increase in state anxiety (immediately after minus before the manipulation) predicted the change in verbal NORD J PSYCHIATRY·VOL 69 NO 6·2015

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33.9 (9.1) 18.6 (3.7) 14.8 (3.3) 11.8 (3.6) 82.3 (14.1) 58.9 (9.2) 12.1 (2.1) 34.6 (1.5) 205.0 (72.4) 23.0 (5.0) 35.5 (8.2) 9.0 (4.7)

15.6 (3.9) 11.0 (2.9) 72.0 (14.2) 56.1 (8.9) 11.5 (2.3) 33.0 (2.2) 208.9 (102.3) 20.1 (6.9) 31.6 (7.7) 10.0 (4.5)

11.9 (6.6)

1.8 (.8)

33.2 (8.0) 17.8 (3.6)

27.1 (9.4)

3.4 (1.6)

7.7 (4.5)

32.4 (8.1)

51.2 (11.7) 10.1 (3.6) 20.2 (6.7)

83.7 (13.7)

15.8 (4.3) 12.0 (2.5)

27.6 (9.3)

4.3 (1.8)

7.0 (4.4)

35.3 (7.8)

56.9 (11.5) 13.3 (2.9) 22.6 (5.1)

90.7 (17.5)

16.2 (3.3) 12.5 (3.5)

11.5 (6.6)

1.7 (.9)

⫺ 2.17***

94.1, ⬍ 0.001

⫺ 0.96* ⫺ 0.97** ⫺ 0.14

18.7, ⬍ 0.001 19.4, ⬍ 0.001 .4, 0.518

0.06

1.63***

53.8, ⬍ 0.001

0.1, 0.734

0.58* 0.82***

6.9, 0.010 14.0, ⬍ 0.001

d

0.1, 0.724

0.4, 0.541

3.3, 0.072 1.6, 0.215 0.8, 0.370

1.4, 0.243

4.0, 0.048 0.6, 0.431

Interaction, F, P

0.09

0.14

0.40 0.28 0.20

0.26

0.44* 0.18

d

0.9, 0.351

[0.2, 0.843] 4.4, 0.038 5.0, 0.028

3.9, 0.049 2.5, 0.120 [⫺ 4.0, ⬍ 0.001]

8.4, 0.005

0.1, 0.814 0.9, 0.347

[⫺ 0.37, 0.714] [⫺ 0.97, 0.342]

Between-group, F, P [t, P]

Results from mixed ANOVAS

0.21

0.04 ⫺ 0.46* ⫺ 0.49*

⫺ 0.44* ⫺ 0.35 ⫺ 0.95***

⫺ 0.64**

0.06 ⫺ 0.21

⫺ 0.08 ⫺ 0.21

d

*P ⬍ 0.05, **P ⬍ 0.01, ***P ⬍ 0.001. s, standard deviation; BSAT, Brixton Spatial Anticipation Test; HC, healthy control; RAVLT, Rey Auditory Verbal Learning Test; RCFT, Rey Complex Figure Test; SAD, social anxiety disorder.

Neuropsychological performance raw scores General cognitive ability Vocabulary Matrix Reasoning Working memory Digit Span Total Letter-Number Sequencing Processing speed Digit-Symbol Coding Verbal learning and memory RAVLT learning RAVLT retention Visuospatial construction and memory RCFT construction accuracy (points) RCFT construction time (seconds) RCFT retention Executive functioning Word fluency total BSAT (errors)

State emotion regulation

State anxiety

Post-anxiety manipulation

SAD, mean (s) HC, mean (s) SAD, mean (s) HC, mean (s) Within-group, F, P

Pre-anxiety manipulation

Table 2. Means and standard deviations for neuropsychological performance raw scores and results from mixed analyses of variance (ANOVAs).

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⫺ 0.33† ⫺ 0.46** ⫺ 0.35* ⫺ 0.15 ⫺ 0.22 ⫺ 0.12 0.13 0.15 0.09 0.02 ⫺ 0.14 ⬍ 0.01

*P ⬍ 0.05, **P ⬍ 0.01. HC, healthy control; SAD, social anxiety disorder. Regarding comorbid diagnoses and medication, a negative correlation refers to a negative association between the presence of a diagnosis or the use of medication and neuropsychological performance. †P ⬍ 0.10,

SAD: ⫺ 0.11; HC: 0.05 SAD: ⫺ 0.19; HC: 0.14 SAD: ⫺ 0.26; HC: ⫺ 0.08 SAD: ⫺ 0.51**; HC: ⫺ 0.29† SAD: ⫺ 0.30†; HC: ⫺ 0.19 SAD: ⫺ 0.09; HC: ⫺ 0.32* SAD: 0.03; HC: ⫺ 0.14 SAD: ⬍ 0.01; HC: 0.03

Average state anxiety Average state emotion suppression Only SAD group Trait social anxiety Trait depression Medication

SAD: ⫺ 0.12; HC: ⫺ 0.29† SAD: ⫺ 0.21; HC: ⫺ 0.27†

⫺ 0.18 ⫺ 0.15 ⫺ 0.20

Word fluency Verbal learning Visuospatial construction accuracy Processing speed

Table 3. Correlations between state factors and neuropsychological performance at baseline.

Visuospatial memory

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learning performance in both the SAD group (r ⫽ ⫺ 0.31, P ⫽ 0.049) and the HCs (r ⫽ ⫺ 0.36, P ⫽ 0.019); the more state anxiety increased, the larger the decrease in verbal learning following the manipulation. One interaction effect was detected, where the SAD group showed a smaller increase on the Digit-Span task than the HCs.

Discussion In accordance with prior studies (8), participants with SAD overall did worse than HCs on the visuospatial test of construction accuracy, visuospatial memory and verbal learning. It was additionally found that participants with SAD performed worse on a test of processing speed and a test of executive functioning (word fluency) than the HCs. The between-group differences on these tasks were statistically significant and of a moderate to large effect size (Cohen’s d ranging from ⫺ 0.44 to ⫺ 0.95). However, only the difference in performance on the visuospatial construction accuracy task was large, corresponding to more than a standard deviation below the HCs’ performance; a difference that may be considered clinically significant (cf. 27). It should be noted that performance on this visuospatial task (RCFT) is not merely reflecting visuospatial functioning, but also may concern executive functions (27), and a similar decrease in performance on the RCFT among individuals with obsessive–compulsive disorder has indeed been interpreted as executive dysfunction (42). Regarding executive functioning, participants with SAD did perform worse than HCs on a measure on word fluency in the present study. Another possible explanation for the decreased visual constructive functioning among individuals with SAD could be their tendency to engage in self-focused attention (43) that likely puts strain on their visual attention capacities. The level of state anxiety was not associated with any of the neuropsychological variables at baseline. However, the anxiety level was rather low with a small variation in both groups of participants (mean [s] on the 1–10-point scale for SAD: 3.4 [1.8]; for HCs: 1.8 [0.8]). Thus, in most participants it may not have reached a level necessary for a negative interference with neuropsychological performance, even in the SAD group. State emotion suppression was negatively associated with visuospatial memory, but only in the HCs, whereas it was negatively associated with verbal learning, only in the SAD group. Thus, the baseline difference between the SAD group and HCs on verbal learning may, partially, be explained by higher levels of emotion suppression in the SAD group. These findings are in accordance with prior studies showing that state emotion suppression is a cognitively taxing emotion regulation strategy, lowering learning and memory performance for emotional material (20–22). The present study extends these findings to also NORD J PSYCHIATRY·VOL 69 NO 6·2015

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cover non-emotional cognitive tasks; however, it should be noted that this was true only for one out of five test performances in each group. Differing effects of the anxiety manipulation were found. A positive effect was found for working memory, processing speed and a test of executive functioning (BSAT). This result could be interpreted as a beneficial effect of state anxiety on performance (cf. 12). However, it could also point to a test–retest effect, although less likely for the working memory and processing speed tests (cf. 17). A negative effect was detected for verbal learning and memory. This effect may be interpreted as state anxiety having a toxic effect on the verbal domain; a notion that is supported by the finding that the magnitude of change in state anxiety corresponded to the magnitude of change in verbal learning; both groups performed worse on verbal learning when they experienced a larger increase in anxiety. Only one interaction effect was found. The SAD group had a smaller increase in performance on the Digit-Span test, indicating that they benefited less from an increase in anxiety. Thus, the hypothesis that an increase in state anxiety in the SAD group, not in HCs, would lead to decreased neuropsychological performance was not confirmed. However, the anxiety manipulation was not very successful in increasing the level of anxiety in the two groups. State emotion suppression did not increase following the anxiety manipulation. Regarding the clinical variables in the SAD group, depressive symptoms and the use of medication were associated with decreased verbal learning performance. In accordance with previous findings (8), the level of social anxiety was not a predictor of neuropsychological test performance, which questions the specificity of the findings. The present study has a number of limitations. The neuropsychological test battery was limited in that it only used one or two tests per assessed function. Moreover, the two groups were not matched on all relevant variables, including age. However, the predictive value of age was explored whenever a between-group difference was detected, and was only found to be positively associated with word fluency, thus, age does not seem to explain this between-group difference. In addition to this, although matched on education, all HCs were actively pursuing an education, which was not the case for all participants with SAD. The response rate was rather low (45%) and one could hypothesize that severe cases chose not to participate, thereby introducing a bias. However, there was no difference on the LSAS score between responders and non-responders, and the mean score on the LSAS was well above the clinical threshold (score ⫽ 85; 44, 45). No reliability measure of the diagnoses given was obtained, but anxiety diagnoses were based on a structured diagnostic interview provided by NORD J PSYCHIATRY·VOL 69 NO 6·2015

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experienced clinicians. Statistically, given the multiple comparisons, the type-1 error could be inflated. However, all significant analyses were evaluated according to the effect size. Moreover, the relatively small sample size introduces some uncertainty when controlling for depressive symptoms. Finally, the anxiety manipulation procedure only resulted in a small increase in state anxiety. In conclusion, participants with SAD showed clinically significant visuospatial construction accuracy difficulties that were not explained by the state factors or clinical variables. The two groups furthermore differed on working memory, processing speed, visuospatial memory and word fluency. State anxiety did not explain any of these between-group differences, whereas the elevated state emotion suppression in the SAD group may explain the difference on verbal learning. Following the anxiety manipulation, the two groups performed better on working memory, processing speed and spatial anticipation, and worse on verbal learning and memory. It is uncertain whether performance improvement reflects a positive effect of anxiety or a test–retest effect, however, the change in state anxiety only predicted the change in verbal learning performance. Contrary to the hypothesis, only one interaction effect (Time⫻ Group) was detected, which may be due to the anxiety manipulation only being moderately effective. It is suggested that future research further investigates visuospatial functioning in SAD by using a variety of tests of the domain in order to come closer to an understanding of this specific cognitive difficulties. In doing this, future studies should include a control group consisting of individuals with other anxiety disorders in order to address the potential specificity to SAD. We also suggest that other relevant state factors, for instance that of adopting and observer’s perspective, are explored. Acknowledgements and disclosures of interest—The authors would like to thank Professor Thomas Nielsen for invaluable comments during the preparation of the manuscript. The study was funded by Aarhus University’s Graduate School of Business and Social Sciences.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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NORD J PSYCHIATRY·VOL 69 NO 6·2015

Neuropsychological test performance in social anxiety disorder.

The effect of state factors on neuropsychological performance in social anxiety disorder (SAD) has not been thoroughly investigated and the overall ne...
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