Schizophrenia Research 159 (2014) 198–204

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Necessary, but not sufficient: Links between neurocognition, social cognition, and metacognition in schizophrenia are moderated by disorganized symptoms Kyle S. Minor a,⁎, Paul H. Lysaker b,c a b c

Department of Psychology, Indiana University—Purdue University Indianapolis, Indianapolis, IN, United States Roudebush VA Medical Center, Indianapolis, IN, United States Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, United States

a r t i c l e

i n f o

Article history: Received 14 June 2014 Received in revised form 10 August 2014 Accepted 13 August 2014 Available online 2 September 2014 Keywords: Schizophrenia Disorganized symptoms Neurocognition Social cognition Metacognition

a b s t r a c t Intact neurocognition has been posited as a necessary, but not sufficient prerequisite for efficient social cognition and metacognition in schizophrenia. Disorganized symptoms likely play a prominent role in these cognitive processes, given the detrimental effects of disorganization on one's ability to synthesize discrete information into an organized whole. However, the relationship between disorganized symptoms and cognitive processes remains unclear. In this study, we examined whether disorganized symptoms: 1) exhibited stronger inverse relationships with cognitive processes than other symptoms, and 2) moderated links between neurocognition and a) social cognition, and b) metacognition. Trained raters assessed psychotic symptoms, neurocognition, social cognition, and metacognition in patients with schizophrenia from a Midwestern VA Medical Center (n = 68) using validated, clinician-rated instruments. We observed significantly greater inverse associations with cognitive processes for disorganized compared to reality distortion symptoms; inverse associations with neurocognition and social cognition were significantly greater for disorganized than negative symptoms. Our hypotheses that disorganized symptoms would moderate relationships between neurocognition and a) social cognition, and b) metacognition were also supported. These findings highlight the importance of disorganized symptoms in elucidating links between neurocognition and social cognitive and metacognitive abilities. Future work should assess whether similar findings occur across the schizophrenia-spectrum, and investigate if targeting disorganization can ameliorate social cognitive and metacognitive impairments in schizophrenia. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Schizophrenia is a debilitating disorder that typically leads to impairments in a wide range of cognitive processes, including neurocognition, social cognition, and metacognition (Frith, 1992; Green, 1996; Penn et al., 1997; Lysaker et al., 2005; Green and Leitman, 2008). The significant heterogeneity found in schizophrenia poses a considerable challenge when assessing impairment in these processes, as no single deficit or symptom affects all, or even most, cases (Cohen and Docherty, 2005; Menezes et al., 2006). One method of accounting for heterogeneity is to group symptoms based on similar putative causes. Although there has been substantial debate on the number of factors in schizophrenia, evidence suggests that the best fitting model includes three symptom clusters: 1) reality distortion (e.g., delusions, hallucinations), 2) negative ⁎ Corresponding author at: IUPUI School of Science, Department of Psychology, LD 124, 402 N. Blackford St., Indianapolis, IN 46202, United States. Tel.: +1 317 274 2933; fax: +1 317 274 6756. E-mail address: [email protected] (K.S. Minor).

http://dx.doi.org/10.1016/j.schres.2014.08.005 0920-9964/© 2014 Elsevier B.V. All rights reserved.

(e.g., anhedonia, alogia), and 3) disorganized (e.g., tangential speech, inappropriate affect; see Liddle, 1987; Cuesta et al., 2007; Malla et al., 1993). Of these, disorganized symptoms have received the least attention, as many early models combined disorganized and reality distortion symptoms to form the positive cluster (Crow, 1980). However, disorganized symptoms have proven to hold important implications in schizophrenia, as their presence is linked with poor occupational functioning (Smith et al., 2002; Evans et al., 2004) and long-term disease course (Shenton et al., 1992; Metsanen et al., 2006). In studies utilizing the three-factor approach, disorganized symptoms appear to be more closely associated with impairments in cognitive processes than reality distortion symptoms. In a meta-analysis conducted by Ventura et al. (2010), disorganized symptoms demonstrated moderate inverse associations with overall neurocognition and neurocognitive functioning across six core domains, whereas reality distortion symptoms were only weakly related. A separate meta-analysis including over 7000 individuals with schizophrenia showed that disorganized symptoms exhibited stronger inverse associations with social cognitive abilities than reality distortion symptoms (Ventura et al., 2013). Metacognition is a third cognitive process where disorganized

K.S. Minor, P.H. Lysaker / Schizophrenia Research 159 (2014) 198–204

symptoms appear to have a more prominent role. Metacognition can be defined as a spectrum of mental activities that involve thinking about thinking (Flavel, 1979; Frith, 1992), ranging from more discrete acts in which people recognize specific thoughts and feelings to more synthetic acts in which an array of intentions, thoughts, feelings, and connections between events are integrated into larger complex representations of others (Semerari et al., 2003; Lysaker et al., 2013; Lysaker and Dimaggio, 2014). It differs from social cognition in that metacognition focuses on synthesizing psychological experiences into mental representations that vary by complexity, adaptiveness and flexibility, whereas social cognition is more concerned with the accuracy of perceptions and representations. Recently, Hamm et al. (2012) observed that disorganized symptoms were inversely linked to metacognition at baseline and six month follow-up and that these associations were considerably greater compared to reality distortion symptoms. Although previous studies have examined the link between disorganized symptoms and cognitive processes, the nature of the relationship between neurocognition, social cognition, and metacognition remains unclear. One area of contention is whether these three cognitive processes are discrete constructs, as each represents trait phenomena that require both lower- and higher-order abilities (Lysaker et al., 2011; Biedermann et al., 2012; Hamm et al., 2012; Ventura et al., 2013). Resolving this issue is critical for delineating whether these constructs should be treated as independent or converging abilities when assessing their impact in schizophrenia. In terms of what is known regarding these relationships, previous studies have observed that neurocognition, social cognition, and metacognition demonstrate moderate correlations with one another, with r-values typically ranging from 0.2 to 0.4 (Hamm et al., 2012; Ventura et al., 2013). However, this indicates that each ability only accounts for approximately 5% to 15% of the variance in the other constructs. Moreover, a number of studies have examined whether these processes can be disentangled from one another, with a growing consensus suggesting that neurocognition, social cognition, and metacognition are related, but independent constructs (Pinkham et al., 2003; Allen et al., 2007; Fanning et al., 2012; Lysaker et al., 2013). Evidence of construct independence informs our understanding of these processes, yet does not clarify their relationship with one another. To date, we know little about how these processes overlap. A theory that has been posited is that intact neurocognition is a necessary, but not a sufficient prerequisite for exhibiting efficient social cognition (Penn et al., 1997; Fanning et al., 2012) and metacognition (Lysaker et al., 2010). One possibility is that the links between these abilities are moderated by additional variables. Understanding how moderators influence links between neurocognition, social cognition, and metacognition is important, as it provides the possibility to discern when relationships between these cognitive processes are strongest. From a clinical standpoint, identifying moderators also offers the potential of clarifying how cognitive processes lead to the social and occupational impairments prevalent in schizophrenia. Disorganized symptoms are prime moderator candidates, given the detrimental effects these symptoms have on one's ability to synthesize discrete information into an organized whole, a critical component of both social cognition and metacognition. This connection between disorganization and cognitive processes was introduced by Bleuler (1911), who believed that brain dysfunction was characterized by a disruption in cognitive processes stemming from a “loosening of associations.” As a result of neurocognitive compromise, the capacity to form the complex thoughts needed to engage in goal-directed behaviors may significantly be disrupted. The “loosening of associations” described by Bleuler is similar to updated models of disorganized symptoms that are currently being examined (see Hardy-Bayle et al., 2003). In this study, we examined whether disorganized symptoms moderated relationships between neurocognition and social cognition and metacognition. To our knowledge, this possibility has not been explored previously.

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1.1. Objectives and hypotheses This study had two primary aims. First, we investigated whether disorganized symptoms exhibited stronger inverse correlations with neurocognition, social cognition, and metacognition compared to other symptom clusters. Our expectation was that associations with each cognitive process would be significantly greater for disorganized than reality distortion symptoms. Second, we aimed to clarify the role of disorganized symptoms in the link between neurocognition and a) social cognition, and b) metacognition. Our hypothesis was that disorganized symptoms would moderate the relationship between neurocognition and both constructs. 2. Method 2.1. Participants Participants were outpatients in a Midwestern VA Medical Center with confirmed DSM-IV-TR (American Psychological Association, 2000) diagnoses of schizophrenia (n = 46) or schizoaffective disorder (n = 22). All participants were in a post-acute phase of illness, with no change in medication, housing, or outpatient status (e.g., hospitalizations) within the past 30 days. Exclusion criteria included active substance dependence or a documented intellectual disability at any time point. This data was part of a larger randomized controlled trial examining the role of cognitive remediation on work outcomes in schizophrenia. For the purposes of this project, we focused solely on participant's baseline scores (i.e., prior to any intervention). To be included in the final sample, participants had to have completed baseline scores for all symptom, neurocognition, social cognition, and metacognition measures (n excluded = 3), resulting in a total of 68 participants. The majority were male (n = 64, 94%), African–American (n = 41, 60%), had received a GED or high school diploma (education M = 12.68, SD = 2.20), were middle-aged (M = 50.50, SD = 10.38), and were hospitalized for the first time in their late twenties (M = 29.15, SD = 12.24). 2.2. Measures Psychotic symptoms were assessed using the Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987), a 30-item scale that was completed by trained research staff following chart review and a semistructured clinical interview. The PANSS has been used in hundreds of studies to assess symptoms and has demonstrated good internal consistency (Kay et al., 1987), interrater reliability (Bell et al., 1992; Lysaker et al., 2013), and predictive validity (Bell et al., 1992). Scores on PANSS items range from 1 to 7, with higher scores indicating greater symptom severity. In this study, we focused on three PANSS factors (see Bell et al., 1994): reality distortion (M = 17.92, SD = 5.12), negative (M = 19.94, SD = 5.09), and disorganized symptoms (M = 16.93, SD = 3.82). The reality distortion category consisted of 6 items (delusions, hallucinations, unusual thought content, somatic concerns, suspiciousness, grandiosity), the negative symptoms included 8 items (passive social withdrawal, emotional withdrawal, blunted affect, lack of spontaneity, poor rapport, disturbances of volition, preoccupation, motor retardation), and the disorganized factor contained 7 items (difficulty in abstract thinking, stereotyped thinking, conceptual disorganization, lack of insight, poor attention, tension, and mannerisms/ posturing). The Measurement and Treatment Research to Improve Cognition in Schizophrenia (MATRICS; Nuechterlein et al., 2008) battery was used to assess neurocognition. The MATRICS was designed to measure neurocognitive ability in schizophrenia; it includes ten subtests across seven neurocognitive domains (processing speed, attention, working memory, verbal learning, visual learning, reasoning and problem solving, and social cognition). In this study, the neurocognition composite

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score contains all MATRICS subtests except the Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT; Mayer et al., 2002), a 29 question measure of emotional processing that was included with social cognition instead of neurocognition measures. MATRICS standardized scores were utilized in all analyses. In addition to the MSCEIT, three measures were used to assess social cognition. These measures reflected three domains (emotion perception, theory of mind, and emotional processing) emphasized in the National Institute of Mental Health's Consensus Committee report on social cognition (Green et al., 2008). The Bell–Lysaker Emotion Recognition Task (BLERT; Bell et al., 1997) assesses emotion perception by presenting 21 behavioral prompts that require participants to choose which emotion (happiness, surprise, disgust, fear, anger, sadness, no emotion) is being demonstrated. Total scores range from 0 to 21 with higher scores indicating greater emotion perception. Theory of mind was assessed using both the Hinting Task (Corcoran et al., 1995; with modifications from Grieg et al., 2004) and the Social Attributions Test— Multiple Choice (SAT-MC; Bell et al., 2010). The Hinting task consists of 10 brief stories where participants are asked to make judgments about a fictional character based on hints in the story. The SAT-MC presents abstract animations to participants and consists of 19 multiple choice questions concerning interactions in these animations. Higher scores indicated greater TOM on both measures. Metacognition was measured using the Metacognition Assessment Scale (MAS-A; Lysaker et al., 2005). MAS-A scores were based on participant responses to the Indiana Psychiatric Illness Interview (IIPI; Lysaker et al., 2002), a semi-structured interview designed to elicit open-ended responses from subjects about how they view their life and deal with mental illness. IPII interviews typically lasted between 30 and 60 min and were conducted by trained clinicians. These interviews were audio taped and transcribed before being rated on the MAS-A (see Lysaker et al., 2005 for protocol information). The MAS-A measures a person's ability to use implicit and explicit information to think about themselves and others in the moment. It consists of a total score and four domain scores: self-reflectivity, awareness of the mind of the other, decentration, and mastery (see Lysaker et al., 2013 for more information). The MAS-A has exhibited good reliability and validity in psychotic populations (Lysaker et al., 2010, 2012).

Table 1 Relationship between symptom dimensions and neurocognition, social cognition, and metacognition (n = 68). Neurocognition

Reality distortion

Negative

Disorganized

Composite Processing speed Attention Working memory Verbal memory Visual memory Reasoning/problem solving

0.11 0.21 0.18 −0.12 0.15 0.19 −0.04

−0.05 −0.19 0.04 −0.10 0.06 −0.08 −0.09

−0.36⁎ −0.27+ −0.28+ −0.43⁎⁎ −0.11 −0.32⁎

Social cognition Composite Emotion perception Theory of mind (hinting) Theory of mind (SAT-MCa) Emotional processing

0.11 0.09 0.09 0.03 0.08

−0.12 −0.09 −0.11 0.04 −0.13

−0.48⁎⁎ −0.36⁎ −0.27+ −0.32⁎ −0.33⁎

Metacognition Total Self Otherb Decentration Mastery

0.21 0.17 0.25+ 0.24 0.12

−0.28+ −0.23+ −0.14 −0.23 −0.32⁎

−0.26+ −0.18 −0.14 0.01 −0.38⁎⁎

−0.14

a

SAT-MC: Social Attributions Test—Multiple Choice. Other: Awareness of the mind of the other. ⁎⁎ p b 0.001. ⁎ p b 0.01. + p b 0.05. b

Disorganized symptoms and the neurocognition composite were centered and entered into step one as predictor variables and their cross product was entered into step two in both analyses. Outcome variables were the social cognition composite in the first regression and the metacognition total in the second regression. An alpha level of .05 was used to determine significance in both analyses.

3. Results 3.1. Correlations between psychotic symptoms and neurocognition, social cognition, and metacognition

2.3. Statistical analyses Data analysis was conducted in four parts. First, composite scores were calculated for neurocognition and social cognition. To create the neurocognition composite, we began by excluding the MSCEIT due to its superior fit with social cognition measures. Next, standardized t scores for all participants were converted to z-scores for the remaining six MATRICS domains. These scores were combined using a weighted average of 1 for each domain. To create the social cognition composite, each of the four social cognition measures was converted to z-scores. Both the BLERT and the MSCEIT were given a weighted average of 1. The Hinting task and SAT-MC were given a weighted average of 0.5, as both assess theory of mind. This provided an equal weight for the three social cognition domains measured in this study (emotion perception, theory of mind, and emotional processing). Second, correlations were conducted to examine which symptom clusters were linked with neurocognition, social cognition, and metacognition. Third, correlations between symptom clusters and each cognitive process total/composite score were compared using Steiger's z transformation (Steiger, 1980). These analyses were conducted by hand, and then checked using an online calculator to control for human error (Lee and Preacher, 2013). To control for multiple comparisons, an alpha level of .01 was set to determine significance for all correlation analyses. Finally, two linear regressions were analyzed to test the hypotheses that disorganized symptoms moderate the relationship between neurocognition and a) social cognition, and b) metacognition.

A correlation matrix was constructed to examine which symptom clusters were significantly related to neurocognition, social cognition, and metacognition (Table 1). Disorganized symptoms exhibited significant inverse correlations with the neurocognition and social cognition composite scores, and an inverse trend level correlation with the metacognition total score. Both disorganized and negative symptoms demonstrated significant inverse relationships with Mastery, one of the four metacognition indices. Reality distortion symptoms were not significantly associated with any clinical variable. These findings supported our expectation that disorganized symptoms would be inversely associated with neurocognitive, social cognitive, and metacognitive variables.

Table 2 Steiger's transformations comparing correlations of symptom dimensions and composite scores (n = 68). Composites

Disorga to RDb z

Disorg to Negc z

Neg to RD z

Neurocognition Social cognition Metacognition

3.21⁎⁎ 4.19⁎⁎ 3.17⁎⁎

2.35⁎ 2.85⁎⁎ −0.15

1.08 1.56 3.42⁎⁎

a

Disorg: Disorganized symptoms. RD: Reality distortion symptoms. Neg: Negative symptoms. ⁎⁎ p b 0.001. ⁎ p b 0.01. b c

K.S. Minor, P.H. Lysaker / Schizophrenia Research 159 (2014) 198–204 Table 3 Disorganized symptoms as a moderating variable in relationships between neurocognition, social cognition, and metacognition (n = 68). Social cognition composite

Metacognition total

Ra

Ra

B

SE B β

B

SE B β

Step 1 .28 .09 Neurocog compositeb .137 .061 .26⁎ .178 .119 .19+ a ⁎⁎ DisorgSx −.222 .067 −.38 −.173 .129 −.17+ Step 2 .34 .14 Neurocog composite .121 .060 .22⁎ .151 .117 .16 DisorgSx −.275 .068 −.47⁎⁎ −.263 .134 −.26⁎ Neurocog × DisorgSx −.155 .067 −.25⁎ −.263 .131 −.25⁎ a

DisorgSx: Disorganized symptoms. Neurocog: Neurocognition. ⁎⁎ p b 0.01. ⁎ p b 0.05. + p b 0.10. b

3.2. Comparing correlations between psychotic symptom clusters and neurocognition, social cognition, and metacognition Associations between symptom clusters were compared to examine the hypothesis that disorganized symptoms would demonstrate stronger inverse correlations with cognitive processes than reality distortion symptoms (Table 2). Inverse associations with all three cognitive processes were significantly greater for disorganized symptoms than reality distortion symptoms. Relationships between neurocognition and social cognition were significantly stronger in disorganized compared to negative symptoms, and negative symptoms exhibited significantly larger inverse correlations with the metacognition total score than reality distortion symptoms. Disorganized and negative symptoms did not significantly differ in their relationship to metacognition.

3.3. Disorganized symptoms as a moderator in the relationship between neurocognition and other cognitive processes Finally, we investigated whether disorganized symptoms moderated the link between neurocognition and a) social cognition, and b) metacognition (Table 3). Neurocognition and disorganized symptoms significantly predicted social cognition in step one of the first regression. After controlling for independent effects of both predictors, the cross product of these variables accounted for a significant decrease in social cognition in step two (see Fig. 1). In the second

Predictor: Neurocognition

β = 0.22

Moderator: Disorganized Symptoms

β = -0.47

Neurocognition X Disorganized Symptoms

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regression, neurocognition and disorganized symptoms significantly predicted metacognition in step one, and their cross product also accounted for significant additional variance in metacognition once independent effects of the predictor variables were controlled for (see Fig. 2). These findings provide evidence for the hypothesis that disorganized symptoms moderate the relationship between neurocognition and other cognitive processes. 4. Discussion Our primary goals in this study were to examine the relationship between disorganized symptoms and neurocognitive, social cognitive and metacognitive abilities, and to clarify whether disorganized symptoms play a role in the link between these cognitive processes. Two key findings emerged. First, disorganized symptoms exhibited significant inverse relationships with all three cognitive processes, and the observed associations were stronger for disorganized symptoms than other psychotic symptoms. Second, disorganized symptoms moderated the pathway between neurocognition and both social cognition and metacognition, which suggests that disorganization is a critical piece connecting these cognitive processes. The observation that disorganized symptoms exhibited greater inverse associations with cognitive processes than reality distortion symptoms supports previous literature (Ventura et al., 2010, 2013; Hamm et al., 2012). Neurocognitive and social cognitive impairments are two of the most commonly observed deficits in schizophrenia (Green, 1996; Penn et al., 1997; Green and Leitman, 2008). Along with metacognition, these constructs represent processes that require the ability to synthesize both lower- and higher-order capacities (Lysaker et al., 2011; Biedermann et al., 2012; Hamm et al., 2012; Ventura et al., 2013). Despite being the focus of many psychopharmacological and psychosocial interventions, results from this study indicate that little overlap may exist between reality distortion symptoms and cognitive processes. This suggests that improving delusions and hallucinations may only have limited effects on addressing impairments in neurocognition, social cognition, and metacognition. Instead, the findings point to the importance of considering how disorganized symptoms affect these cognitive processes. Unexpectedly, we observed that disorganized symptoms were more strongly associated with neurocognition and social cognition than negative symptoms. This differs from previous meta-analyses where significant differences were not found (Dibben et al., 2008; Ventura

Outcome: Social Cognition

β = -0.25

Fig. 1. Disorganized symptoms moderate the relationship between neurocognition and social cognition.

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Predictor: Neurocognition

β = 0.16

Moderator: Disorganized Symptoms

β = -0.26

Neurocognition X Disorganized Symptoms

Outcome: Metacognition

β = -0.25

Fig. 2. Disorganized symptoms moderate the relationship between neurocognition and metacognition.

et al., 2013). One explanation for the difference in findings could be that previous meta-analyses may have included studies that used different models to separate symptoms. For example, some studies might have excluded disorganized symptoms as a distinct category and included some of these symptoms (e.g., difficulty in abstract thinking) in the negative symptom category. A second potential explanation is that participants in this study exhibited a low rate of primary negative symptoms. Individuals with pronounced primary negative symptoms, commonly referred to as the deficit syndrome (Carpenter et al., 1988), tend to show higher rates of neurocognitive and social cognitive impairments than those who display mostly secondary negative symptoms (Buchanan et al., 1994; Galderisi et al., 2002). Although the distinction between primary and secondary negative symptoms was not assessed here, all participants in this sample had to agree to take part in a twoyear therapeutic intervention as part of a longitudinal study of vocational outcomes. This likely resulted in a low rate of participation among deficit patients. Replication should be sought in a study that assesses primary negative symptoms and does not require additional participation in a long-term intervention. The most substantial finding in this study was that disorganized symptoms moderated relationships between neurocognition, social cognition, and metacognition. Previous studies have provided evidence that neurocognition is a necessary but not sufficient prerequisite for exhibiting efficient social cognition and metacognition (Penn et al., 1997; Lysaker et al., 2010; Fanning et al., 2012). Our results suggest that disorganized symptoms are an integral link in these pathways, with increasing disorganization resulting in a weaker association between cognitive processes. Whereas Bleuler (1911) viewed disorganization as the variable that led to dysfunctions in cognitive processes, the findings here propose that it is a moderating variable that influences the relationship between neurocognition, social cognition, and metacognition. To our knowledge, this is the first study to report this finding. A strength of this study is that the primary constructs (e.g., psychotic symptoms, neurocognition, social cognition, and metacognition) were assessed across multiple domains, which allowed us to examine how separate facets of each construct were related to other variables of interests. However, one limitation is that no behavioral measures were utilized to assess psychotic symptoms. Although clinician-rated instruments are commonly used in schizophrenia studies, behaviorallybased instruments have demonstrated promise as assessment tools, particularly in identifying disorganized symptoms (Docherty, 2012; Minor and Cohen, 2012). The lack of a patient control group is another limitation of this study. Attenuated levels of disorganization and impairments in cognitive processes have been observed in other psychiatric populations (Docherty et al., 1996; Lysaker et al., 2014); comparing

these relationships using a psychiatric control group could provide insight into whether disorganization serves as a moderating variable across groups, or whether this finding is specific to schizophrenia. A third limitation of this study is that the majority of participants had been diagnosed with schizophrenia for several years. Thus, the findings might not generalize to more recently diagnosed individuals. An additional issue pertains to the directionality of our findings. Although not a limitation of study design, one might question whether cognitive impairment could lead to greater disorganized symptoms. Clinical high risk studies have demonstrated that attenuated symptoms and cognitive deficits are both present in high risk cohorts prior to diagnosis of psychotic disorders, with cognitive functioning, much like symptoms, resting between that of healthy controls and individuals who have transitioned into their first episode of psychosis (Simon et al., 2007; Woodberry et al., 2010; Giuliano et al., 2012). Determining whether disorganized symptoms or cognitive impairments precede the other construct is outside the scope of this study, but remains an important issue for future studies. In line with previous literature (Klingberg et al., 2006), we conceptualized schizophrenia symptoms and cognitive impairments as independent constructs in the current study. Future research should address study limitations while pursuing several exciting avenues generated from this study. One area to investigate is the role of disorganized symptoms in neurocognition, social cognition, and metacognition at different points on the schizophreniaspectrum. Examining whether disorganized symptoms moderate these cognitive processes in psychometric schizotypy, clinical high risk, and first episode psychosis populations would provide important clinical information regarding which stage moderation effects emerge. In many of these populations, little work has been conducted on the cognitive processes studied here, particularly metacognition. A recent study observed that metacognitive deficits are present in first episode psychosis (Vohs et al., 2014); however, a paucity of studies have analyzed these deficits in individuals at risk for psychosis. Thus, a related line of inquiry could assess metacognition in clinical high risk and psychometric schizotypy samples. Another area to pursue is how to disentangle the role of specific disorganized symptoms in neurocognition, social cognition, and metacognition. Previous research has highlighted the importance of specific disorganization symptoms functioning (Bowie and Harvey, 2008; see Silverstein and Keane, 2011), and testing these relationships with cognitive processes is warranted. Implementing behavioral instruments to investigate whether certain symptoms (e.g., disorganized speech, perceptual organization) drive the relationships observed in this study is one approach that should be used. Finally, it is critical to assess how the moderation effects

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found here can be used to reduce the debilitating impairments in cognitive processes observed in patients. With replication our findings may have clinical implications. For instance, they point to the need to develop and test strategies to target disorganized symptoms in order to assist individuals with schizophrenia to develop greater capacity for social cognition and metacognition. Role of funding source Funding for this study was provided by a grant (D6629R) from the Rehabilitation Research and Development Service, U.S. Department of Veterans Affairs. The IRB had no further role in designing this study, or in collection, interpretation, or analysis of data, in writing of the manuscript, or in the decision to submit the finished manuscript for publication. Contributors Kyle S. Minor conducted the literature search, performed data analysis, and wrote or co-wrote all drafts of the manuscript. In addition, he assisted in the design of the study. Paul H. Lysaker supervised the data collection, assisted with study design, and coauthored all drafts of the manuscript. Conflict of interest Both authors declare no conflicts of interest in the current study. Acknowledgments We wish to thank all of the patients who participated in this study, as well as the graduate students and staff who helped collect this data.

References Allen, D.N., Strauss, G.P., Donohue, B., van Kammen, D.P., 2007. Factor analytic support for social cognition as a separable cognitive domain in schizophrenia. Schizophr. Res. 93, 325–333. American Psychological Association, 2000. Diagnostic and Statistical Manual of Mental Disorders, 4th ed.—text revision. Author, Washington, DC. Bell, M., Milstein, R., Beam-Goulet, J., Lysaker, P., Cicchetti, D., 1992. The Positive and Negative Syndrome Scale and the Brief Psychiatric Rating Scale: reliability, comparability, and predictive validity. J. Nerv. Ment. Dis. 180, 723–728. Bell, M.D., Lysaker, P.H., Goulet, J.B., Milstein, R.M., Lindenmayer, J.P., 1994. Five component model of schizophrenia: assessing the factorial invariance of the PANSS. Psychiatr. Res. 52, 295–303. Bell, M.D., Bryson, G.J., Lysaker, P.H., 1997. Positive and negative affect recognition in schizophrenia: a comparison with substance abuse and normal control subjects. Psychiatr. Res. 73, 73–82. Bell, M.D., Fiszdon, J.M., Greig, T.C., Wexler, B.E., 2010. Social attribution test—multiple choice (SAT-MC) in schizophrenia: comparison with community sample and relationship to neurocognitive, social cognitive and symptom measures. Schizophr. Res. 122, 164–171. Biedermann, F., Frajo-Apor, B., Hofer, A., 2012. Theory of mind and its relevance in schizophrenia. Curr. Opin. Psychiatr. 25, 71–75. Bleuler, E., 1911. Dementia Praecox or the Group of Schizophrenia. (J. Zinkin, Trans.). International Universities Press, New York. Bowie, C.R., Harvey, P.D., 2008. Communication abnormalities predict functional outcomes in chronic schizophrenia: differential associations with social and adaptive functions. Schizophr. Res. 103, 240–247. Buchanan, R.W., Strauss, M.E., Kirkpatrick, B., Holstein, C., Breier, A., Carpenter, W.T., 1994. Neuropsychological impairments in deficit vs nondeficit forms of schizophrenia. Arch. Gen. Psychiatr. 51, 804–811. Carpenter, W.T., Heinrichs, D.W., Wagman, A.M., 1988. Deficit and nondeficit forms of schizophrenia: the concept. Am. J. Psychiatr. 145, 578–583. Cohen, A.S., Docherty, N.M., 2005. Symptom-oriented versus syndrome approaches to resolving heterogeneity of neuropsychological functioning in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 17, 384–390. Corcoran, R., Mercer, G., Frith, C., 1995. Schizophrenia, symptomatology and social inference: investigating theory of mind in people with schizophrenia. Schizophr. Res. 24, 397–405. Crow, T.J., 1980. Molecular pathology of schizophrenia: more than one disease process? Br. Med. J. 280, 66–68. Cuesta, M.J., Ugarte, M.D., Goicoa, T., Eraso, S., Peralta, V., 2007. A taxometric analysis of schizophrenia symptoms. Psychiatr. Res. 150, 245–253. Dibben, C.R., Rice, C., Laws, K., McKenna, P.J., 2008. Is executive impairment associated with schizophrenic syndromes? A meta-analysis. Psychol. Med. 39, 1–12. Docherty, N.M., 2012. On identifying the processes underlying schizophrenic speech disorder. Schizophr. Bull. 38, 1327–1335. Docherty, N.M., Hawkins, K.A., Hoffman, R.E., Quinlan, D.M., Rakfeldt, J., Sledge, W.H., 1996. Working memory, attention, and communication disturbances in schizophrenia. J. Abnorm. Psychol. 105, 212–219. Evans, J.D., Bond, G.R., Meyer, P.S., Kim, H.W., Lysaker, P.H., Gibson, P.J., Tunis, S., 2004. Cognitive and clinical predictors of success in vocational rehabilitation in schizophrenia. Schizophr. Res. 70, 331–342. Fanning, J.R., Bell, M.D., Fiszdon, J.M., 2012. Is it possible to have impaired neurocognition but good social cognition in schizophrenia? Schizophr. Res. 135, 68–71.

203

Flavel, J.H., 1979. Metacognition & cognitive monitoring: a new area of cognitivedevelopmental inquiry. Am. Psychol. 34, 906–911. Frith, C.D., 1992. The Cognitive Neuropsychology of Schizophrenia. Lawrence Erlbaum Associates, Sussex. Galderisi, S., Maj, M., Mucci, A., Cassano, G.B., Invernizzi, G., Rossi, A., Vita, A., Dell'Osso, L., Daneluzzo, E., Pini, S., 2002. Historical, psychopathological, neurological, and neuropsychological aspects of deficit schizophrenia: a multicenter study. Am. J. Psychiatr. 159, 983–990. Giuliano, A.J., Li, H., Mesholam-Gately, R.I., Sorenson, S.M., Woodberry, K.A., Seidman, L.J., 2012. Neurocognition in the psychosis risk syndrome: a quantitative and qualitative review. Curr. Pharm. Des. 18, 399–415. Green, M.F., 1996. What are the functional consequences of neurocognitive deficits in schizophrenia? Am. J. Psychiatr. 153, 321–330. Green, M.F., Leitman, D.I., 2008. Social cognition in schizophrenia. Schizophr. Bull. 34, 670–672. Green, M.F., Penn, D.L., Bentall, R., Carpenter, W.T., Gaebel, W., Gur, R.C., Kring, A.M., Park, S., Silverstein, S.M., Heinssen, R., 2008. Social cognition in schizophrenia: an NIMH workshop on definitions, assessment, and research opportunities. Schizophr. Bull. 34, 1211–1220. Grieg, T.C., Bryson, G.J., Bell, M.D., 2004. Theory of mind performance in schizophrenia: diagnostic, symptoms, and neuropsychological correlates. J. Nerv. Ment. Dis. 192, 12–18. Hamm, J.A., Renard, S.B., Fogley, R.L., Leonhardt, B.L., Dimaggio, G., Buck, K.D., Lysaker, P.H., 2012. Metacognition and social cognition in schizophrenia: stability and relationship to concurrent and prospective symptom assessments. J. Clin. Psychol. 68, 1303–1312. Hardy-Bayle, M.C., Sarfati, Y., Passerieux, C., 2003. The cognitive basis of disorganization symptomatology in schizophrenia and its clinical correlates: toward a pathogenetic approach to disorganization. Schizophr. Bull. 29, 459–471. Kay, S.R., Fizszbein, A., Opler, L.A., 1987. The positive and negative syndrome scale for schizophrenia. Schizophr. Bull. 13, 261–276. Klingberg, S., Wittorf, A., Wiedemann, G., 2006. Disorganization and cognitive impairment in schizophrenia: independent symptom dimensions? Eur. Arch. Psychiatry Clin. Neurosci. 256, 532–540. Lee, I.A., Preacher, K.J., 2013. Calculation for the Test of the Difference between Two Dependent Correlations with One Variable in Common, (September, Retrieved from http://quantpsy.org). Liddle, P.F., 1987. The symptoms of chronic schizophrenia: a re-examination of the positive–negative dichotomy. Br. J. Psychiatry 151, 145–151. Lysaker, P.H., Dimaggio, G., 2014. Metacognitive capacities for reflection in schizophrenia: implications for developing treatments. Schizophr. Bull. 40, 487–491. Lysaker, P.H., Clements, C.A., Plasck-Hallberg, C.D., Knipscheer, S.J., Wright, D.E., 2002. Insight and personal narratives of illness in schizophrenia. Psychiatry 65, 197–206. Lysaker, P.H., Carcione, A., Dimaggio, G., Johannesen, J.K., Nicolo, G., Procacci, M., Semerari, A., 2005. Metacognition amidst narratives of self and illness in schizophrenia: associations with neurocognition, symptoms, insight, and quality of life. Acta Psychiatr. Scand. 112, 64–71. Lysaker, P.H., Erickson, M.A., Buck, K.D., Procacco, M., Nicolo, G., Dimaggio, G., 2010. Metacognition in schizophrenia spectrum disorders: methods of assessment and associations with neurocognition and functioning. Eur. J. Psychiatr. 24, 220–226. Lysaker, P.H., Erickson, M., Ringer, J., Buck, K.D., Semerari, A., Carcione, A., Dimaggio, G., 2011. Metacognition in schizophrenia: the relationship of mastery to coping, insight, self-esteem, social anxiety, and various facets of neurocognition. Br. J. Clin. Psychol. 50, 412–424. Lysaker, P.H., Ringer, J.M., Buck, K.D., Grant, M., Olesek, K., Leudtke, B.L., Dimaggio, G., 2012. Metacognitive and social cognition deficits in patients with significant psychiatric and medical adversity: a comparison between participants with schizophrenia and a sample of participants who are HIV-positive. J. Nerv. Ment. Dis. 200, 130–134. Lysaker, P.H., Gumley, A., Luedtke, B., Buck, K.D., Ringer, J.M., Olesek, K., Kukla, M., Leonhardt, B.L., Popolo, R., Dimaggio, G., 2013. Social cognition and metacognition in schizophrenia: evidence of their independence and linkage with outcomes. Acta Psychiatr. Scand. 127, 239–247. Lysaker, P.H., Vohs, J., Hamm, J.A., Kukla, M., Minor, K.S., de Jong, S., van Donkersgoed, R., Pijnenborg, M.H., Kent, J.S., Matthews, S.C., Ringer, J.M., Leonhardt, B.L., Francis, M.M., Buck, K.D., Dimaggio, G., 2014. Deficits in metacognitive capacity distinguish patients with schizophrenia from those with prolonged medical adversity. J. Psychiatr. Res. 55, 126–132. Malla, A.K., Ross, M.G., Norman, P.W., Cortese, L., Diaz, F., 1993. Three syndrome concept of schizophrenia: a factor analytic study. Schizophr. Res. 10, 143–150. Mayer, J.D., Salovey, P., Caruso, D.R., 2002. Mayer–Salovey–Caruso Emotional Intelligence Test (MSCEIT): User's Manual. Multi-Health Systems, Inc., Toronto, ON. Menezes, N.M., Arenovich, T., Zipursky, R.B., 2006. A systematic review of longitudinal outcome studies of first-episode psychosis. Psychol. Med. 36, 1349–1362. Metsanen, M., Wahlberg, K.E., Hakko, H., Saarento, O., Tienari, P., 2006. Thought Disorder Index: a longitudinal study of severity levels and schizophrenia factors. J. Psychiatr. Res. 40, 258–266. Minor, K.S., Cohen, A.S., 2012. The role of atypical semantic activation and stress in odd speech: implications for individuals with psychometrically defined schizotypy. J. Psychiatr. Res. 46, 1231–1236. Nuechterlein, K.H., Green, M.F., Kern, R.S., Baade, L.E., Barch, D.M., Cohen, J.D., Essock, S., Fenton, W.S., Frese, F.J., Gold, J.M., Goldberg, T., Heaton, R.K., Keefe, R.S., Kraemer, H., Mesholam-Gately, R., Seidman, L.J., Stover, E., Weinberger, D.R., Young, A.S., Zalcman, S., Marder, S.R., 2008. The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. Am. J. Psychiatr. 165, 203–213.

204

K.S. Minor, P.H. Lysaker / Schizophrenia Research 159 (2014) 198–204

Penn, D.L., Corrigan, P.W., Bentall, R.P., Racenstein, J., Newman, L., 1997. Social cognition in schizophrenia. Psychol. Bull. 121, 114–132. Pinkham, A.E., Penn, D.L., Perkins, D.O., Lieberman, J., 2003. Implications for the neural basis of social cognition for the study of schizophrenia. Am. J. Psychiatr. 160, 815–824. Semerari, A., Carcione, A., Dimaggio, G., Falcone, M., Nicolo, G., Procacci, M., Alleva, G., 2003. How to evaluate metacognitive functioning in psychotherapy? the metacognitive assessment scale and its applications. Clin. Psychol. Psychother. 10, 238–261. Shenton, M.E., Kikinis, R., Jolesz, F.A., Pollak, S.D., LeMay, M., Wible, C.G., Hokama, H., Martin, J., Metcalf, D., Coleman, M., McCarley, R.W., 1992. Abnormalities of the left temporal lobe and thought disorder in schizophrenia: a quantitative MRI study. N. Engl. J. Med. 327, 604–612. Silverstein, S.M., Keane, B.P., 2011. Perceptual organization impairment in schizophrenia and associated brain mechanisms: review of research from 2005 to 2010. Schizophr. Bull. 37, 690–699. Simon, A.E., Cattapan-Ludewig, K., Zmilacher, S., Arbach, D., Gruber, K., Dvorsky, D.N., Roth, B., Isler, E., Zimmer, A., Umbricht, D., 2007. Cognitive functioning in the schizophrenia prodrome. Schizophr. Bull. 33, 761–771.

Smith, T.E., Hull, J.W., Huppert, J.D., Silverstein, S.M., 2002. Recovery from psychosis in schizophrenia and schizoaffective disorder: symptoms and neurocognitive ratelimiters for the development of social behavioral skills. Schizophr. Res. 55, 229–237. Steiger, J.H., 1980. Tests for comparing elements of a correlation matrix. Psychol. Bull. 87, 245–251. Ventura, J., Thames, A.D., Wood, R.C., Guzik, L.H., Hellemann, G.S., 2010. Disorganization and reality distortion in schizophrenia: a meta-analysis of the relationship between positive symptoms and neurocognitive deficits. Schizophr. Res. 121, 1–14. Ventura, J., Wood, R.C., Hellemann, G.S., 2013. Symptom domains in neurocognitive functioning can help differentiate social cognitive processes in schizophrenia: a metaanalysis. Schizophr. Bull. 39, 102–111. Vohs, J.L., Lysaker, P.H., Francis, M.M., Hamm, J., Buck, K.D., Olesek, K., Outcalt, J., Dimaggio, G., Leonhardt, B., Liffick, E., Meydiyoun, N., Breier, A., 2014. Metacognition, social cognition, and symptoms in patients with first episode and prolonged psychoses. Schizophr. Res. 153, 54–59. Woodberry, K.A., Seidman, L.J., Giuliano, A.J., Verdi, M.B., Cook, W.L., McFarlane, W.R., 2010. Neuropsychological profiles in individuals at clinical high risk for psychosis: relationship to psychosis and intelligence. Schizophr. Res. 123, 188–198.