Intact motivated attention in schizophrenia: Evidence from event-related potentials

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Abstract

Emotionally significant stimuli typically capture attention (called motivated attention) even when they are irrelevant to tasks where attention is directed. Previous studies indicate that several components of emotional processing are intact in schizophrenia when subjects are instructed to attend to emotionally-evocative stimuli. However, few studies have examined whether emotional stimuli capture attention to a normal degree in people with schizophrenia when attention is directed elsewhere. The current event-related potential study examined motivated attention to task-irrelevant emotional stimuli in 35 stabilized outpatients and 26 healthy controls with a modified visual P300 oddball detection task. Participants viewed images of rare target and commonly occurring standard letter stimuli, as well as intermixed emotional (unpleasant, pleasant, neutral) pictures. Subjects were instructed to count the number of rare targets; the emotional valence of the picture stimuli was, therefore, task-irrelevant. We separately evaluated the Early Posterior Negativity (EPN) and Late Positive Potential (LPP) to emotional pictures and the P300 to target stimuli. Patients and controls showed similar patterns of EPN and LPP amplitude to the emotional stimuli, such that the EPN and LPP were larger for both pleasant and unpleasant versus neutral pictures. Although patients performed worse than controls on the target counting task, both groups showed comparable P300 differentiation between target versus non-target stimuli. Emotional stimuli captured attentional resources in people with schizophrenia even when the emotional stimuli were task-irrelevant, suggesting intact motivated attention at the level of early electrophysiological responding.

Introduction

People with schizophrenia often show diminished emotional expression and pleasurable experiences based on clinical rating scales (Blanchard et al., 2011). However, when directly exposed to evocative stimuli (e.g., pictures, foods), patients show normal emotion-modulated experiential, cardiovascular, electrodermal, and startle eyeblink responses (Kring and Moran, 2008). Motivationally relevant stimuli rarely present themselves in this way in daily life; they are often incidental to the primary tasks we are performing. In healthy subjects, incidental emotional stimuli naturally capture attention, an adaptive process called “motivated attention” (Bradley, 2009). Adaptive functioning, however, requires an optimal balance: incidental emotional stimuli need to capture attention but not deplete the resources required for ongoing goal-directed pursuits. The current study used an event-related potential (ERP) paradigm to evaluate processing of task irrelevant emotional stimuli in schizophrenia.

In healthy subjects, two ERPs, the early posterior negativity (EPN) and late positive potential (LPP), are larger for both pleasant and unpleasant compared with neutral pictures, reflecting increased attention to motivationally relevant stimuli (see Hajcak et al., 2010). The EPN (200–300 ms) reflects early and relatively automatic selective attentional processing, whereas the LPP (400–1000 ms) reflects more sustained allocation of attentional resources. Consistent with the concept of motivated attention, the EPN and LPP are larger for emotional than neutral pictures even when the valence of pictures is irrelevant to the primary task to which attention is directed (Hajcak et al., 2010).

Recently, we found patients showed generally normal early and late ERP's to emotional versus neutral pictures during a task in which subjects attended to the pictures (Horan et al., 2010). However, we are not aware of any prior studies that examined whether patients also show intact ERPs to task-irrelevant emotional images. To address this question, the current study used a modified visual P300 task modeled on Fichtenholtz et al. (2004) that involved rare target letter stimuli intermixed with irrelevant images of varying emotional content. A handful of behavioral and functional magnetic resonance imaging (fMRI) studies show mixed evidence of intact versus impaired automatic emotional processing in schizophrenia (e.g., Dichter et al., 2010, Roux et al., 2010, Schwartz et al., 2010, Strauss et al., 2011); our prior ERP study led to the prediction that patients would show a larger EPN and LPP to task-irrelevant emotional versus neutral stimuli, similar to healthy controls.

Section snippets

Participants

Thirty-five outpatients with schizophrenia based on the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID; First et al., 1996). Patients were medicated at clinically determined dosages. Psychiatric symptoms were rated using the expanded 24-item Brief Psychiatric Rating Scale (BPRS; Kopelowicz et al., 2008). Twenty-five healthy controls from the local community were screened with the SCID and SCID-II (Cluster A). Procedures were approved by the local Institutional Review Board.

ERP's to pictures

Grand average ERPs are presented in Fig. 2, Fig. 3, and mean ERP amplitudes are presented in Table 2. For the EPN, a 3 (Valence) × 2 (Group) repeated-measures ANOVA revealed a significant Valence effect. Compared to neutral pictures, LPP was significantly more positive for both unpleasant, t(60) = 5.23, p < .001, and pleasant pictures, t(60) = 4.38, p < .001, which did not significantly differ from each other, t(60) = 1.39, p > .05. The Group and Interaction effects were not significant, indicating a similar

Discussion

This study found normal early and late emotion-modulated ERPs in schizophrenia. Hence, the results from our earlier study (Horan et al., 2010) extend to processing task-irrelevant emotional stimuli. Automatic “grabbing” of attention by, and sustained processing of, emotional stimuli may reflect yet another area of relatively preserved emotion processing in schizophrenia. Our paradigm also allowed us to evaluate performance and ERPs in the target detection task where attention was directed. The

Role of funding sources

This work was supported by a NARSAD Young Investigator Award (to WPH) and the National Institute of Mental Health (MH082782 to WPH; MH065707, MH43292 to MFG). Funding sources had no role in study design or in the collection, analysis and interpretation of data; or in the writing of this report.

Contributors

Drs. Horan, Hajcak, and Green designed the study. All authors contributed to data analysis and intepretation. Dr. Horan wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.

Conflict of interest

None.

Acknowledgments

The authors would like to thank and acknowledge the following people who contributed to the data collection for the study: Mark McGee, Crystal Gibson, Cory Tripp, Katie Weiner, and Poorang Nori.

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