Actively paranoid patients with schizophrenia over attribute anger to neutral faces

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Abstract

Previous investigations of the influence of paranoia on facial affect recognition in schizophrenia have been inconclusive as some studies demonstrate better performance for paranoid relative to non-paranoid patients and others show that paranoid patients display greater impairments. These studies have been limited by small sample sizes and inconsistencies in the criteria used to define groups. Here, we utilized an established emotion recognition task and a large sample to examine differential performance in emotion recognition ability between patients who were actively paranoid (AP) and those who were not actively paranoid (NAP). Accuracy and error patterns on the Penn Emotion Recognition test (ER40) were examined in 132 patients (64 NAP and 68 AP). Groups were defined based on the presence of paranoid ideation at the time of testing rather than diagnostic subtype. AP and NAP patients did not differ in overall task accuracy; however, an emotion by group interaction indicated that AP patients were significantly worse than NAP patients at correctly labeling neutral faces. A comparison of error patterns on neutral stimuli revealed that the groups differed only in misattributions of anger expressions, with AP patients being significantly more likely to misidentify a neutral expression as angry. The present findings suggest that paranoia is associated with a tendency to over attribute threat to ambiguous stimuli and also lend support to emerging hypotheses of amygdala hyperactivation as a potential neural mechanism for paranoid ideation.

Introduction

Emotion recognition impairments and their relationship to social and functional outcome are well established in schizophrenia (Couture et al., 2006, Kohler et al., 2010, Pinkham et al., 2007). It remains unclear however whether the degree of these impairments may differ between symptom based subgroups and specifically between patients who experience prominent paranoid symptoms and those who do not. Previous investigations of the influence of paranoia on facial affect recognition in schizophrenia have provided conflicting results. Some studies support an advantage for paranoid over non-paranoid patients (Chan et al., 2008, Davis and Gibson, 2000, Lewis and Garver, 1995, Phillips et al., 1999, Van't Wout et al., 2007), while others show the opposite pattern (An et al., 2006, Russell et al., 2007, Williams et al., 2007). Kline et al. (1992) note that this pattern may differ based on emotion, as their work showed that paranoid patients were more accurate for negative emotions but that groups did not differ in correctly labeling positive emotions.

These discrepancies may be partially explained by the fact that all of the above studies utilized relatively small samples (generally fewer than 20 individuals per group); however, methodological differences between studies also deserve consideration. Perhaps most importantly, many previous studies have defined the paranoid and non-paranoid subgroups based on diagnostic subtype rather than symptom ratings at the time of testing (An et al., 2006, Chan et al., 2008, Davis and Gibson, 2000, Lewis and Garver, 1995, Van't Wout et al., 2007). It is important to note that under DSM-IV-TR, patients do not require persecutory or paranoid delusions to be diagnosed with this subtype. Therefore, much of the previous work may not have examined paranoia per se. Additionally, the range of emotions studied and the tasks used to measure emotion recognition ability have varied widely between studies.

The potential role of paranoia in emotion recognition is also raised by several neuroimaging studies showing differences in amygdala functioning between individuals with prominent paranoid symptoms at the time of scanning and those without. The amygdala is thought to play a key role in emotion perception (Adolphs, 2002, Gur et al., 2002, Loughead et al., 2008, Vuilleumier and Pourtois, 2007) and has also been linked to the processing of threat (Ohman, 2005) and complex social judgments (Adolphs et al., 1998, Winston et al., 2002). fMRI studies indicate that paranoid patients generally show reduced amygdala activation as compared to non-paranoid patients (Phillips et al., 1999, Pinkham et al., 2008a, Pinkham et al., 2008b, Russell et al., 2007, Williams et al., 2004, Williams et al., 2007), a finding that would seem to contradict behavioral reports of increased recognition accuracy for paranoid patients. Of note, however, each of these imaging studies has assigned individuals to groups based on clinical ratings of paranoia as opposed to diagnostic subtype, and these studies have largely used tasks of implicit emotion recognition (e.g. asking participants to identify the gender of an emotional face) rather than the explicit identification of emotion utilized in behavioral tasks. While differences in task demands may partially explain the unexpected result of reduced amygdala activation in paranoid patients, tasks of explicit emotion recognition administered after scanning do show greater impairments in paranoid patients (Russell et al., 2007, Williams et al., 2004, Williams et al., 2007), suggesting that reduced amygdala activation may indeed be related to poorer performance.

In an effort to complement the neuroimaging findings, and to address the discrepancies in previous behavioral studies, we utilized an established emotion recognition task and a large sample to assess facial affect recognition abilities in patients with schizophrenia who were actively paranoid and those who were not actively paranoid. Groups were defined based on the presence of paranoid ideation at the time of testing rather than diagnostic subtype. Based on the above-mentioned findings of reduced amygdala activation in paranoid patients, we hypothesized that actively paranoid patients would be impaired relative to patients who were not actively paranoid in emotion identification accuracy.

Section snippets

Participants

Archival data from 132 individuals with schizophrenia were utilized for the present investigation. All individuals were volunteers at the Schizophrenia Research Center of the University of Pennsylvania Medical Center who had provided written informed consent to participate in studies that were approved by the University of Pennsylvania ethics review board. Diagnoses were confirmed with the Diagnostic Interview for Genetics Studies (DIGS; (Nurnberger et al., 1994) and medical history

Primary analyses

Contrary to our prediction that AP patients would be impaired relative to NAP patients on emotion recognition accuracy, the main effect of group was not significant (F(1,128) = .26, p = .61, ηp2 = .002) indicating that the two patient groups did not differ overall. There was however a main effect of emotion (F(3.16,404.43) = 9.12, p < .001, ηp2 = .066) such that accuracy for happy was better than all other emotions (p < .001 for all comparisons) and accuracy for anger was worse than all other emotions (p < 

Discussion

The current study assessed potential differences in emotion recognition ability between actively paranoid and non-paranoid patients with schizophrenia. Patients who were paranoid at the time of testing, relative to those who were not, showed a specific impairment in the ability to accurately identify neutral facial expressions. An analysis of error patterns revealed that this impairment was due to a greater tendency for AP patients to incorrectly attribute anger to neutral faces. These findings

Role of funding source

Funding for this project was provided by the National Institute of Mental Health grants R01 MH60722 (RCG) and T32 MH19112 (REG). These sources had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Contributors

Author 1 (A. Pinkham) aided in study design, oversaw and completed all statistical analyses, wrote the first draft of the manuscript, and contributed substantially to all subsequent drafts of the manuscript. Author 2 (C. Brensinger) aided in study design, complied all data, and assisted with statistical analysis. Author 3 (C. Kohler) aided in study design, assisted with original data collection, and edited drafts of the manuscript. Author 4 (R. E. Gur) aided in study design, provided study

Conflict of interest

All authors report no conflicts of interests.

Acknowledgements

We gratefully acknowledge all of the individuals who provided data for the present study.

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