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. Author manuscript; available in PMC: 2021 Aug 1.
Published in final edited form as: J Abnorm Psychol. 2020 Jun 11;129(6):670–676. doi: 10.1037/abn0000580

NEUROPHYSIOLOGICAL EVIDENCE FOR EMOTION REGULATION IMPAIRMENT IN SCHIZOPHRENIA: THE ROLE OF VISUAL ATTENTION AND COGNITIVE EFFORT

Lisa A Bartolomeo 1, Adam J Culbreth 2, Kathryn L Ossenfort 3, Gregory P Strauss 1,*
PMCID: PMC7440778  NIHMSID: NIHMS1618129  PMID: 32525326

Abstract

Prior research indicates that individuals with schizophrenia (SZ) display emotion regulation abnormalities that are critically linked to increased symptom severity and poor functional outcome. However, processes contributing to the aberrant implementation of various strategies are unclear. The current study took a multi-modal approach to identifying mechanisms underlying the impaired implementation of two strategies: reappraisal and distraction. Participants included 25 individuals with SZ and 25 healthy controls (CN) who completed separate event-related potential (ERP) and eye-tracking/pupil dilation tasks. On each task, participants were required to either passively view unpleasant or neutral stimuli or reduce negative affect using reappraisal or distraction emotion regulation strategies. The late positive potential (LPP) event related potential component was used as an objective neurophysiological indicator of emotion regulation effectiveness. Eye-tracking and pupil dilation were used to determine whether the implementation of reappraisal and distraction were associated with abnormal patterns of visual attention and reduced cognitive effort, respectively. Results indicated that CN could effectively decrease the amplitude of the LPP for both reappraisal and distraction compared to unpleasant passive viewing; however, individuals with SZ showed comparable LPP amplitude among conditions, indicating a failure to effectively implement these strategies. In CN, successful down regulation of negative affect was associated with different patterns of visual attention across regulation strategies. During reappraisal, there was an increase in fixations to arousing scene regions, whereas distraction was associated with reduced attention to arousing interest areas. In contrast, individuals with SZ made fewer fixations to arousing interest areas during reappraisal and more fixations to arousing interest areas during distraction. Furthermore, pupil dilation results suggested that individuals with SZ failed to exert adequate effort while implementing reappraisal. Collectively, these findings suggest that individuals with SZ are ineffective at implementing reappraisal and distraction; dysfunctional patterns of visual attention and low cognitive effort may contribute to these difficulties.

Keywords: Reappraisal, Distraction, Pupil Dilation, Eye Tracking, Effort, Attention, Psychosis

General Scientific Summary

Emotion regulation abnormalities are a core feature of schizophrenia that are linked to poor clinical and psychosocial functioning. The current study extends previous findings of impaired down-regulation of behavioral and physiological responses to negative emotional stimuli in schizophrenia and suggests that aberrant visual attention and deficient cognitive effort may underlie this impairment.

Introduction

There has been increased interest in determining the nature and significance of emotion regulation abnormalities in schizophrenia (SZ). A large number of studies have examined habitual emotion regulation strategy use in SZ. Results of these studies provide relatively consistent evidence that SZ report a reduction in the frequency of using adaptive strategies (e.g., reappraisal) and increased use of maladaptive strategies (e.g., suppression). Importantly, this pattern predicts a range of poor clinical outcomes, suggesting that emotion regulation is a key treatment target in SZ (for a review and meta-analysis see O’Driscoll, Laing, Mason, 2014).

Few studies have used objective laboratory-based measures to examine emotion regulation in SZ. Four published studies used electroencephalography (EEG) and examined the late positive potential (LPP) event related potential (ERP) component as an objective index of emotion regulation effectiveness. The LPP is a centroparietal midline ERP component that becomes evident at approximately 300ms and persists as a greater relative positivity for emotional than neutral stimuli until stimulus offset (Hajcak et al., 2010). Although healthy individuals are able to augment the LPP using a variety of strategies, individuals with SZ are less able to do so (Horan et al., 2013; Strauss et al., 2013; Strauss et al., 2015; Sullivan & Strauss, 2017). Similar findings have been observed in fMRI studies, where individuals with SZ and individuals at high-risk for psychosis have demonstrated hypofrontality while implementing reappraisal (Larabi, van der Meer, Pijnenborg, Ćurčić-Blake, & Aleman, 2018; Morris, Sparks, Mitchell, Weickert, & Green, 2012; van der Meer et al., 2014; van der Velde et al., 2015; Zhang et al., 2020). These neural abnormalities have been associated with heightened negative affect (Strauss et al., 2013; Sullivan & Strauss, 2017), but direct associations with symptoms have not been observed (Horan et al., 2013; Morris et al., 2012; Strauss et al., 2013; Strauss et al., 2015; Sullivan & Strauss, 2017; van der Meer et al., 2014).

Factors leading individuals with SZ to be less effective at implementing various emotion regulation strategies to change the neural response to unpleasant stimuli are unclear. One prior study identified dysfunctional patterns of visual attention and low effort as key components of ineffective emotion regulation when people with SZ were asked to implement a directed attention strategy (Strauss et al., 2015). However, it is unclear whether these two factors are actually critical to emotion regulation implementation failures because directed attention is a strategy that conflates visual attention and effort with the implementation of the strategy itself. Thus, the question of whether visual attention and effort are core moderators of emotion regulation abnormalities has therefore not been adequately tested.

To more conclusively address this question, it is necessary to use a paradigm requiring participants to implement two different strategies that require differing levels of effort and distinct patterns of visual attention. Prior studies suggest that distraction and reappraisal are good candidates for this purpose. In a prior eye tracking and pupillometry study on healthy individuals, Strauss, Ossenfort, and Whearty (2016) demonstrated that successful down regulation of negative affect was associated with different patterns of visual attention across regulation strategies. During reappraisal, attention was initially directed to arousing scene regions and subsequently shifted away later in the trial, whereas in distraction, there was decreased attention to arousing interest areas across the whole trial. Pupil dilation was higher for reappraisal than distraction or unpleasant passive viewing, suggesting that reappraisal requires high amounts of cognitive effort. These findings suggest that distraction and reappraisal necessitate different patterns of visual attention and effort to be effective, making them good candidates to explore moderators of emotion regulation ineffectiveness in SZ.

In the current study, we used EEG, eye tracking, and pupillometry to determine whether dysfunctional visual attention and low effort contribute to ineffective use of reappraisal and distraction in SZ. The following hypotheses were evaluated:

  1. SZ will fail to report as much of a decrease in negative emotion while attempting reappraisal and distraction relative to unpleasant passive viewing compared to controls (CN).

  2. CN will display lower LPP amplitude for reappraisal and distraction compared to unpleasant passive viewing, suggesting effective implementation; however, SZ will display similar LPP amplitudes for unpleasant passive viewing, reappraisal, and distraction.

  3. In emotional areas of interest (E-AOIs), CN will have fewer fixations while attempting reappraisal and distraction than unpleasant passive viewing; however, SZ will have more fixations in distraction and reappraisal than unpleasant passive viewing.

  4. CN will display greater pupil dilation for reappraisal than unpleasant passive viewing, and less pupil dilation for distract than unpleasant passive viewing; however, SZ will display comparable pupil dilation for reappraisal, distraction, and unpleasant passive viewing.

  5. Emotion regulation abnormalities will be associated with increased negative affect, more severe symptoms, functional impairment, and cognitive deficits in SZ.

Method

Participants

Twenty-five individuals meeting DSM-IV-TR criteria for schizophrenia (SZ) and 25 control participants without a current psychiatric diagnosis (CN) completed the study. Participants provided written informed consent following the University of Maryland Institutional Review Board guidelines and received financial compensation for their participation. SZ and CN did not differ on age, parental education, sex, or ethnicity. CN had significantly greater personal education, as expected (see Table 1).

Table 1.

Demographic Characteristics

SZ CN Test Statistic p-value
Age 37.2 (12.9) 39.9 (11.1) F = 00.59 p = 0.45
Parental Education 13.5 (3.5) 14.7 (2.8) F = 01.7 p = 0.19
Participant Education 13.4 (1.8) 15.6 (2.1) F = 13.36 p < 0.01
% Male 69.6% 70.8% χ2 = 00.01 p = 0.92
Race χ2 = 02.02 p = 0.73
 Caucasian 56.5% 58.3%
 African-American 34.8% 33.3%
 Asian-American 00.0% 04.2%
 American-Indian 04.3% 00.0%
 Biracial 04.3% 04.2%
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Note. SZ = schizophrenia group; CN = control group; MCCB = MATRICS Consensus Cognitive Battery; BNSS = Brief Negative Symptom Scale; BPRS = Brief Psychiatric Rating Scale; LOF = Level of Function Scale.

SZ were recruited through the Outpatient Research Program at the Maryland Psychiatric Research Center and evaluated during a period of clinical stability, as evidenced by no changes in medication type or dosage for a period greater than or equal to four weeks. Consensus diagnosis was established via a best-estimate approach based upon multiple interviews and a detailed psychiatric history retrieved from medical records review. Diagnoses were subsequently confirmed using the Structured Clinical Interview for DSM-IV (SCID) (First, Spitzer, Gibbon, & Williams, 2002) by research staff trained to reliability standards.

CN were recruited through the use of random digit dialing, word-of-mouth, and newspaper advertisements. Exclusionary criteria for CN included current Axis I or II diagnoses as determined by the SCID (First et al., 2002) and SCID-P (Pfohl, Blum, & Zimmerman, 1997), a family history of psychosis, and currently taking psychotropic medications. All participants were free from neurological injury or disease, medical disorders that could interfere with test results (e.g., cancer, infectious disease, sleep apnea), and did not meet criteria for substance abuse or dependence within the last six months.

Procedures

Before completing the experimental procedures, research staff trained to reliability standards conducted SCID-I and SCID-II semi-structured clinical interviews to assess for Axis I and II diagnoses. To evaluate symptom severity in the SZ group, the following interviews were conducted: Brief Psychiatric Rating Scale (BPRS; (Overall & Gorham, 1962), Brief Negative Symptom Scale (BNSS; (Kirkpatrick et al., 2010) and Level of Function Scale (LOF; (Hawk, Carpenter, & Strauss, 1975). Cognitive functioning was assessed via the MATRICS Consensus Cognitive Battery (MCCB; (Nuechterlein et al., 2008). Participants completed separate ERP and eye tracking emotion regulation tasks, which were counterbalanced in order.

Details of the EEG task are provided in Thiruchselvam et al. (2011) and details of the eye tracking task and data processing procedures are provided in Strauss et al. (2016).

EEG Recording and Data Processing Procedures

In a room shielded from electromagnetic interference, participants completed the emotion regulation task while EEG was recorded from Ag/AgCl electrodes mounted in an elastic cap using a subset of the International 10/20 System (Fz, C3, Cz, C4, CPz, P3, Pz, P4, Oz, Fp1, Fp2, and left mastoid). Data was collected online using a right mastoid reference, and then re-referenced offline to the average of the left and right mastoids. The horizontal electrooculogram (HEOG) measured horizontal eye movements via electrodes placed lateral to the external canthi. Vertical EOG captured blinks and vertical eye movements with an electrode placed below the left eye. Electrode impedances were maintained below 15 KΩ throughout the recording. The EEG and EOG were amplified by a Neuroscan Synamps amplifier with a gain of 5000, a bandpass filter of 0.05–100 Hz, and a 60-Hz notch filter. The amplified signals were digitized at 500 Hz and averaged offline.

All signal processing and analysis procedures were performed in Matlab using EEGLAB toolbox and ERPLAB toolbox (http://www.erpinfo.org/erplab). Data preprocessing consisted of visual inspection to manually remove instances of EMG artifact and extreme offsets. Independent component analysis (ICA) was then used to identify and correct artifact induced by eye blinks during the recording. ICA-corrected data was then segmented into epochs spanning 200 prior to the onset of the stimulus to 5000 ms post-stimulus onset that were also baseline corrected. ERP data from three participants in the SZ group were excluded due to poor data quality (i.e., poor signal-to-noise ratio defined by < 50% of segments remaining after processing).

ERP Measurement Procedures

ERPs were constructed by taking the grand average of all trials within each of the four conditions (unpleasant passive, neutral, reappraise, distract). The LPP was measured across electrode sites Cz and CPz, as the average amplitude between 300–5000ms post-stimulus onset where the effect was maximal. Measurement procedures were consistent with prior work in this area and this particular task (Hajcak et al., 2010; Strauss et al., 2013; Sullivan & Strauss, 2017).

Eye Tracking Apparatus

Eye position and pupil dilation were recorded monocularly from the right eye at 2000 Hz using an SR Research Eyelink 1000 desk-mounted system. A 9-point calibration was used and drift-correction was performed prior to each trial. Participants were seated 70 cm from a 17” monitor operating at a refresh rate of 60 Hz, with head positioned in a chin-and-forehead rest to reduce motion artifacts. Pupil activity was examined in Eyelink’s scaled pupil diameter values rather than absolute sizes or percent change from baseline fixation. Scaled values generally ranged between 1000 to 3000, which corresponds to approximately to 1–3 mm.

Data Analysis

To evaluate hypotheses 1–4, difference scores were calculated to isolate regulation relative to reactivity. For self-report, ERP, and eye tracking variables, the difference score was calculated as unpleasant passive – regulation condition, with higher scores reflecting better regulation for self-report and ERPs and fewer relative fixations for regulation than unpleasant passive in eye tracking variables. To isolate reactivity, a difference scores of unpleasant passive – neutral was calculated. One-way ANOVAs were used to examine group differences in ERP, eye tracking, and pupil measures of difference scores for measures of emotion regulation and reactivity. Bivariate correlations were used to evaluate hypothesis 5 regarding associations between experimental and clinical variables. Evaluation of skewness and kurtosis indicated that transformations were not necessary for any of the analyses.

Results

Hypothesis 1: Self-Report

Data from the eye tracking and EEG tasks was averaged to create subjective measures of emotional reactivity and regulation. One-way ANOVA indicated that SZ had poorer subjective emotion regulation than CN for reappraisal and a trend for distraction, but groups did not differ in emotional reactivity (see Table 2).

Table 2.

Subjective and Objective Emotional Reactivity and Regulation

CN M (SD) SZ M (SD) Test-Statistic P-value Partial eta squared
Self-Report
 Unpleasant Passive - Neutral 2.21 (.52) 2.24 (.68) F (1,43) = 0.03 p =0.87 0.87
 Unpleasant Passive - Reappraise .87 (.64) .47 (.51) F (1,43) =5.42 p =.03 0.12
 Unpleasant Passive - Distract .83 (.77) .42 (.64) F (1,43) = 3.57 p = .07 0.08
Event Related Potentials
 Unpleasant Passive - Neutral 6.38 (6.59) 5.83 (9.06) F (1, 43) = 0.05 p = 0.82 0.001
 Unpleasant Passive - Reappraise 2.64 (4.80) −.01 (4.99) F (1, 43) = 3.24 p = 0.08 0.07
 Unpleasant Passive - Distract 4.55 (5.73) −.75 (4.19) F (1, 43) = 12.05 p < 0.001 0.22
Pupil Dilation
 Unpleasant Passive - Neutral −3.51 (73.22) −37.20 (67.36) F (1, 46) = 2.67 p = .11 0.06
 Reappraise - Unpleasant Passive 62.58 (65.41) 22.73 (66.52) F (1, 46) = 4.27 p = .04 0.09
 Distract - Unpleasant Passive −48.30 (107.72) −18.60 (58.80) F (1, 46) = 1.32 p = .26 0.03
Eye Tracking Total Fixations
 Unpleasant Passive - Neutral .64 (2.02) 1.48 (1.62) F (1, 46) = 2.40 p = .13 0.05
 Unpleasant Passive - Reappraise −.17 (1.47) .63 (1.09) F (1, 46) = 4.40 p = .04 0.09
 Unpleasant Passive - Distract 3.19 (2.50) 1.30 (1.85) F (1, 46) = 8.39 p = .01 0.16
Eye Tracking E-AOI Fixations
 Unpleasant Passive - Reappraise −1.53 (.55) −1.40 (.60) F (1, 45) = 0.58 p = .45 0.01
 Unpleasant Passive - Distract 3.19 (2.50) 1.30 (1.85) F (1, 45) = 7.01 p = .01 0.14
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Note. SZ = schizophrenia group; CN = control group.

Hypothesis 2: Event Related Potentials

SZ and CN did not differ on emotional reactivity (unpleasant passive – neutral). However, SZ had significantly lower LPP difference score for reappraisal than CN and a trend toward a lower difference score for distraction. These findings indicate a neurophysiological emotion regulation abnormality in SZ (see Table 2 and Figure 1).

Figure 1.

Figure 1

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LPP Grand Average Waveforms by Group and Condition Note. SZ = Schizophrenia group; CN = Control group; LPP = Late positive potential.

Hypothesis 3: Pupil Dilation

There was a significant group difference for the reappraise-unpleasant passive difference score, but not the distract – unpleasant passive difference score, suggesting that SZ exert less effort while implementing reappraisal than CN (see Table 2).

Hypothesis 4: Eye Tracking

To examine global differences in visual attention across viewing conditions, fixation count was calculated by collapsing across the entire 5 second period, with the image border serving as the boundary for the AOI. SZ had fewer relative fixations during reappraisal and more relative fixations during distraction than CN.

EAOI analyses were calculated to evaluate attention to arousing areas of interest. Groups did not differ for reappraisal; however, SZ had more relative fixations in arousing EAOIs for distraction than CN (see Table 2).

Hypothesis 5: Correlations

State and Trait Affect

In SZ, greater state negative emotional reactivity to stimuli was associated with lower neural emotional reactivity for unpleasant stimuli (r = −0.50, p = 0.04). Poorer subjective use of reappraisal was associated with more relative fixations during reappraisal trials (r = 0.50, p = 0.02). Poorer subjective use of distraction was associated with more total fixations for distraction (r = 0.57, p = 0.01). Greater trait negative affect was associated with fewer total fixations for unpleasant passive viewing (r = −0.45, p = 0.04) and more total fixations within emotional interest areas during reappraisal (r = 0.52, p = 0.02).

In CN, greater state negative emotional reactivity was associated with poorer neurophysiological emotion regulation for reappraisal (r = 0.44, p = 0.04). Poorer subjective emotion regulation during distraction was associated with more total fixations (r = 0.44, p = 0.04) and more fixations within arousing interest areas while implementing distraction (r = 0.44, p = 0.04).

Clinical Measures

In SZ, higher negative symptoms were associated with fewer relative fixations during reappraisal (r = −0.49, p = 0.02) and poorer subjective emotion regulation during reappraisal (r = −0.57, p = 0.01). Better total functional outcome was associated with greater effort/pupil dilation during reappraisal (r = 0.49, p = 0.02), greater subjective negative emotional reactivity (r = 0.44, p = 0.049), and better subjective emotion regulation during reappraisal (r = 0.47, p = 0.03). Higher positive symptoms were associated with greater effort during reappraisal (r = −0.45, p = 0.04). Higher disorganization was associated with poorer neurophysiological emotion regulation for reappraisal (r = −0.63, p = 0.002) and fewer relative fixations during reappraisal (r = −0.43, p = 0.048). Higher BPRS total scores were associated with lower effort during reappraisal (r = −0.51, p = 0.01). Global cognition on the MCCB was not significantly associated with any experimental task variables.

Task Variables

In SZ, greater neurophysiological negative emotion reactivity was associated with more total fixations for unpleasant relative to neutral stimuli (r = 0.50, p = 0.03). Neurophysiological emotion regulation for reappraisal and distraction were not associated with eye tracking or pupil variables.

Discussion

The current study evaluated the effectiveness of reappraisal and distraction emotion regulation strategies in individuals with SZ by examining subjective and objective markers of emotion regulation. Several important findings emerged.

First, ERP data provided further evidence for a neurophysiological emotion regulation abnormality in SZ. Both groups displayed intact emotional reactivity, demonstrated by larger LPP amplitude in response to unpleasant compared to neutral stimuli. Although controls had lower LPP amplitude when implementing distraction and reappraisal than during unpleasant passive viewing (i.e., suggesting successful emotion regulation), individuals with SZ did not. These findings add to a growing body of research from ERP and fMRI studies indicating that individuals with SZ are ineffective at decreasing the neurophysiological response to unpleasant stimuli for reappraisal and directed attention strategies (Horan et al., 2013; Morris et al., 2012; Strauss et al., 2013; Strauss et al., 2015; van der Meer et al., 2014; Zhang et al., 2020). The current findings extend these results, indicating that ineffective implementation also occurs for distraction.

Second, pupillometry data provided evidence that insufficient effort allocation may contribute to abnormal emotion regulation in SZ. Past emotion regulation studies have demonstrated that relative to unpleasant passive viewing, implementation of reappraisal results in greater pupil dilation, whereas implementation of distraction requires less pupil dilation (Strauss et al., 2016; Urry et al., 2006; van Reekum et al., 2007). These findings suggest that reappraisal is a relatively effortful strategy, whereas distraction is not. The current findings replicated this pattern of pupil response in CN. In contrast, individuals with SZ did not display increased pupil dilation while implementing reappraisal compared to unpleasant passive viewing, suggesting that inadequate cognitive effort expenditure may underlie impaired implementation of this strategy. This is consistent with results from Strauss et al. (2015), which found that individuals with SZ had reduced pupil dilation compared to CN when implementing a demanding directed attention strategy that required high cognitive effort. However, SZ did not display reduced allocation of effort during distraction, a less effortful strategy. Interestingly, EMA findings have shown that individuals with SZ self-report greater amounts of effort expenditure during emotion regulation than CN (Visser et al., 2018). The discrepancy between these findings and our pupil results suggests that either individuals with SZ have limited insight into the amount of effort exerted, or that the subjective and objective measures of effort used in these studies reflect different constructs. Subjective reports may correspond to the desire to control emotional responding, whereas pupil dilation may reflect the amount of cognitive effort required to implement a strategy.

Third, eye-tracking data provided evidence that abnormal patterns of visual attention also contribute to aberrant emotion regulation in SZ. Consistent with a prior eye-tracking study on healthy undergraduates incorporating the same paradigm (Strauss et al., 2016), important differences emerged when comparing visual scanning patterns across the four trial types in CN. Distraction was associated with decreased attention within EAOIs and fewer global fixations, suggesting that effective implementation of this strategy involves orienting attention away from aversive content and dwelling on less arousing regions. Reducing total visual scanning may be adaptive during distraction, allowing healthy individuals to conserve cognitive resources needed to generate mental representations of neutral content. Reappraisal was associated with a different pattern of visual attention than distraction, with CN exhibiting longer dwell time within EAOIs during reappraisal than unpleasant passive viewing. This pattern suggests that effective reappraisal involves directing attention towards arousing content in order to generate an alternative interpretation of the image. SZ did not display this pattern of visual attention while implementing emotion regulation strategies. SZ fixated longer within EAOIs than CN when applying distraction, and had fewer fixations on EAOIs while attempting to implement reappraisal. These findings suggest that individuals with SZ display ineffective patterns of visual attention during reappraisal and distraction, allocating too little and too much attention to arousing interest areas while attempting to implement these strategies, respectively.

Certain limitations should be considered. First, EEG has excellent temporal resolution, but relatively poor spatial resolution. This limits conclusions about specific neural circuits contributing to the LPP abnormalities observed here; future fMRI studies using these paradigms are therefore warranted. Second, how to interpret the nonsignificant correlations with clinical and experimental measures is unclear. Our sample size was low, resulting in reduced power. However, there appears to be an emerging pattern of null associations between ERP emotion regulation indicies and clinical measures across studies, suggesting that it may be necessary to further validate the presumed clinical significance of ERP measures.

Despite these limitations, the current results have important implications. First, leading explanations of the origins of SZ propose a critical role for stress reactivity in the vulnerability for psychosis (Corcoran et al., 2003). The current results add to the growing body of evidence suggesting that it is not just stress reactivity, but also the ability to regulate or control the stress response that is abnormal in SZ. This suggests that prevailing theoretical accounts of stress-vulnerability should be updated to incorporate emotion regulation abnormalities. Second, the earlier results of Strauss et al. (2015) did not definitively indicate that visual attention and effort were critical mechanisms underlying emotion regulation failures. The experimental manipulation of reappraisal and distraction in the current study provided clear evidence for a role of effort and visual attention, which reflect novel mechanisms that could be targeted in future interventions. Third, psychosocial and computerized cognitive training interventions have been developed to treat emotion regulation abnormalities, targeting visual attention and effort mechanisms (Cohen & Ochsner, 2018; Sanchez-Lopez, Everaert, Van Put, De Raedt, & Koster, 2019; Wadlinger & Isaacowitz, 2011). These interventions have demonstrated efficacy for enhancing emotion regulation but they have yet to be applied to SZ. The current findings suggest that such treatments may offer promise; however, they would need to be modified for use in this population.

Funding source:

Research was supported by grant K23-MH092530 from NIMH to GPS.

Footnotes

Disclosures: GPS was one of the original developers of the BBSS and receives royalties in relation to its commercial use that are donated to brain and behavioral research foundation. GPS has consulted for or received speaking or travel honorarium from MedAvante-Prophase, Minerva, Lundbeck, and Acadia.

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