Schizophrenia Research 161 (2015) 210–214

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Functional and structural brain asymmetries in patients with schizophrenia and bipolar disorders Céline Royer a, Nicolas Delcroix b, Elise Leroux a,c, Mathieu Alary a, Annick Razafimandimby a,d, Perrine Brazo a,c,e, Pascal Delamillieure a,c,e, Sonia Dollfus a,c,e,⁎ a

CNRS, UMR 6301 ISTCT, ISTS Team, GIP CYCERON, Bd Henri Becquerel, BP5229, F-14074 Cedex Caen, France CNRS, UMS 3408, GIP CYCERON, Bd Henri Becquerel, BP5229, F-14074 Cedex Caen, France CHU de Caen, Service de Psychiatrie, Centre Esquirol, Caen, F-14000, France d Université de Caen Basse-Normandie, IBFA, Caen, F-14000, France e Université de Caen Basse-Normandie, UFR de médecine (Medical School), Caen, F-14000, France b c

a r t i c l e

i n f o

Article history: Received 14 June 2014 Received in revised form 15 November 2014 Accepted 15 November 2014 Available online 2 December 2014 Keywords: Schizophrenia Bipolar disorders Language Functional hemispheric lateralization Gray matter volume asymmetry MRI

a b s t r a c t Objectives: This study aimed to compare the functional and gray matter asymmetries in patients with schizophrenia (SZ), patients with bipolar disorders (BD), and healthy controls (HCs) to test whether decreased leftward functional hemispheric lateralization and gray matter volume asymmetry could mark the boundary between schizophrenia and bipolar disorder. Methods: A total of 31 right-handed SZ and 20 right-handed BD underwent a session of functional MRI with a speech listening paradigm. Participants were matched with HCs for gender, age, and education. Functional laterality indices (FLI) and gray matter volume asymmetry indices (GVAI) were computed from the individual functional language network. Correlations between the FLI and GVAI indices were also examined. Results: SZ exhibited significantly decreased leftward functional hemispheric lateralization whereas BD did not. The GVAIs did not differ significantly between SZ and HCs or between BD and HCs. There were positive correlations between GVAIs and FLIs in all groups. Conclusions: Loss of laterality for language comprehension with retention of gray matter volume asymmetry indicates that gray matter loss alone will not account for the pathophysiology of schizophrenia. Impaired leftward functional hemispheric lateralization for language but not gray matter volume asymmetry can be considered a biomarker of SZ. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Specificity of cerebral markers in patients with schizophrenia (SZ) or bipolar disorders (BD) must be considered in light of the debate on the nosological delimitation of the two disorders (Lake and Hurwitz, 2007). Few functional magnetic resonance imaging studies investigating language networks have sought to identify cerebral biomarkers to discriminate these patient groups (McIntosh et al., 2008; Maïza et al., 2010; Whalley et al., 2012). Nevertheless, some authors have reported Abbreviations: AHRS, Auditory Hallucinations Rating Scale; ARS, Association de Recherche pour la Schizophrénie; BD, bipolar disorders; CS, comprehension score; DSMIV, Diagnostic and Statistical Manual of Mental Disorder 4th edition; FLI, functional laterality index; FLIint, intermediate functional laterality index; FWE, family-wise error; GVAI, gray matter volume asymmetry index; GVAIint, intermediate gray matter volume asymmetry index; HC, healthy control; HCL-20, hypomania checklist; HRSD, Hamilton Rating Scale for Depression; MNI, Montreal Neurological Institute; MRI, magnetic resonance imaging; nCS, normalized comprehension score; PANSS, Positive and Negative Syndrome Scale; SPM, Statistical Parametric Mapping; SZ, schizophrenia. ⁎ Corresponding author at: Centre Esquirol, CHU Caen, Caen 14000, France. Fax: +33 231068749. E-mail address: [email protected] (S. Dollfus).

http://dx.doi.org/10.1016/j.schres.2014.11.014 0920-9964/© 2014 Elsevier B.V. All rights reserved.

decreased leftward functional lateralization for language in SZ patients (Sommer et al., 2003; Dollfus et al., 2005; van Veelen et al., 2011; Sheng et al., 2013), and one previous study suggested that change in functional hemispheric lateralization for language could be a biomarker of SZ (Alary et al., 2013b). However, gray matter volume changes in language structures in SZ and BD patients have been little investigated (Ratnanather et al., 2013). Therefore, the present study compared functional and gray matter asymmetries among SZ patients, BD patients, and healthy controls (HCs). We hypothesized that decreased leftward functional hemispheric lateralization and gray matter volume asymmetry in a language network would be specifically observed in SZ patients but not in BD patients. 2. Materials and methods 2.1. Participants A total of 31 SZ and 20 BD (Diagnostic and Statistical Manual of Mental Disorder 4th Edition; DSM-IV) were included after giving informed written consent and with the agreement of the local ethics

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committee. All participants were right-handed. In the current study, we used a sample expanded from a previous study (Alary et al., 2013b) to increase the number of BD and SZ. Moreover, each group of patients was carefully matched with HCs for gender, age, and education level (Table 1). The clinical state of SZ was evaluated with the Positive and Negative Syndrome Scale (PANSS) (Kay et al., 1987) and the Auditory Hallucinations Rating Scale (AHRS) (Hoffman et al., 2003). The clinical state of BD was assessed using the Hamilton Rating Scale for Depression (HRSD) (Hamilton, 1960) and the hypomania checklist (HCL-20) (Angst, 1992). All patients were stabilized, with no change in treatment during the preceding month.

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2.5. FLIs The FLIs were computed according to the bootstrap approach of Wilke and Lidzba's toolbox (Wilke and Lidzba, 2007). Considering the 5000 most activated voxels in both hemispheres of the brain and discarding the clusters smaller than 50 voxels, the intermediate FLIs (FLIint) were calculated with the following formula: FLIint ¼

Right activation‐Left activation : Right activation þ Left activation

Then, the final FLI was generated as the threshold weighted mean of the FLIint (Wilke and Schmithorst, 2006):

2.2. Language task The experimental paradigm consisted of listening to a factual story told in French. The reference task was to listen to the same story in Tamil, a language not known to French nationals. The stimuli were presented in a block design for 5 min, alternating 32-s blocks in French or Tamil (Tzourio et al., 1998). Participants were instructed to listen passively and attentively with the eyes closed. After scanning, participants were asked to answer a comprehension questionnaire (maximal score 20) to evaluate their involvement in the task (Table 1). 2.3. Data acquisition Anatomical T1-weighted and T2-weighted volumes and functional T2*-weighted volumes were acquired using a 3-T scanner (IRM Philips Achieva, Netherlands). These data were pre-processed using SPM5 subroutines (Statistical Parametric Mapping, UK), allowing us to obtain the anatomical and functional images used for the following analyses in the MNI template (Montreal Neurological Institute, Canada).

X ðFLIint  thresholdÞ X FLI ¼ : threshold The index resulted in negative values for predominantly leftward lateralization and positive values for rightward lateralization. 2.6. GVAIs The calculation of the GVAIs was adapted from the threshold independent method used for the FLIs (Wilke and Lidzba, 2007). The masked individual contrast maps were thresholded and applied on the individual gray matter map to obtain the gray matter volumes for each participant (Fig. 1). This last step was repeated at 100 different thresholds, equally distributed from 0 to the maximum t-value (Wilke and Schmithorst, 2006; Wilke and Lidzba, 2007). For each threshold, an intermediate GVAI (GVAIint) was calculated with the following formula:

2.4. Data analysis A map of “French minus Tamil” blood oxygen level-dependent (BOLD) signal contrast was generated for each subject with SPM5. Then, two mean t-maps were generated: one with the data from SZ and their respective, matched HCs, and one with the data from the BD and their respective, matched HCs (SPM5, one-sample t-test, threshold at p b 0.05, corrected by family-wise error, FWE, k = 200 voxels, excluding the cerebellum). Both maps were symmetrized to yield two masks, one for SZ and their matched controls (mask 1, n = 62) and one for BD and their matched controls (mask 2, n = 52). To compute the functional laterality indices (FLIs) and gray matter volume asymmetry indices (GVAIs), the individual contrast maps were masked with either mask 1 or mask 2 (Fig. 1).

GVAIint ¼

Right GM volume‐Left GM volume : Right GM volume þ Left GM volume

Then, final GVAI was generated, as the threshold weighted mean of the GVAIint: X ðGVAIint  thresholdÞ X : GVAI ¼ threshold The index resulted in positive values for rightward structural asymmetry and negative values for leftward structural asymmetry.

Table 1 Characteristics of patients with schizophrenia (SZ) or with bipolar disorders (BD) and their matched controls (HCs).

Age, y Male sex, n (% of total) Education level, y Edinburgh score Comprehension score Illness duration, y Total PANSS AHRS score HRSD score HCL-20 score FLIs GVAIs

SZ (n = 31)

HCs matched with SZ (n = 31)

BD (n = 20)

HCs matched with BD (n = 32)

33.9 ± 5.9 20 (64.5) 12.3 ± 1.9 93.8 ± 10.6 9.8 ± 4.6 a 8.8 ± 4.9 57.3 ± 16.0 13.9 ± 13.6 – – −0.23 ± 0.4 a −0.42 ± 0.4

35.2 ± 9.3 20 (64.5) 12.4 ± 2.3 94.0 ± 13.7 14.5 ± 2.5 – – – – – −0.40 ± 0.2 −0.55 ± 0.3

44.7 ± 9.3 9 (45) 12.5 ± 2.5 96.0 ± 9.1 11.7 ± 4.0 b 16.2 ± 10.2 – – 3.4 ± 3.4 2.5 ± 3.7 −0.34 ± 0.4 −0.50 ± 0.4

42.1 ± 7.7 15 (47) 12.2 ± 2.0 93.8 ± 11.8 14.1 ± 3.2 – – – – – −0.30 ± 0.4 −0.44 ± 0.5

Significance level at p b 0.05; mean ± standard deviation unless otherwise noted. PANSS = Positive and Negative Syndrome Scale; AHRS = Auditory Hallucinations Rating Scale; FLIs = functional lateralization index; GVAIs = gray matter volume asymmetry index. a Statistical significance between SZ and HCs matched with SZ. b Significance between BD and HCs matched with BD.

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Fig. 1. Steps for calculating the gray matter volume asymmetry index. First, an individual “French minus Tamil” functional map is generated (1). Second, two masks are processed; they correspond to 2 symmetrized mean t-maps: one with the individual maps from SZ patients and their respective matched HCs (mask 1, only display (2) in the figure), and one with the individual maps from the BD patients and their respective matched HCs (mask 2) (p b 0.05, corrected by FWE). Third, each individual functional map was masked by mask 1 (only displayed (3) on the figure) or mask 2. Then, at one given threshold, the individual gray matter map (4) was masked by this functional map (3) generating an anatomical map (5) allowing the calculation of an intermediate GVAI. This last step was repeated at 100 different thresholds, equally distributed from 0 to the maximum t-value to generate the final GVAI. GM = gray matter; GVAIint = intermediate gray matter volume asymmetry index.

2.7. Statistical analysis The FLI and GVAI values were subjected to a Fisher transformation to normalize the variables, and the comprehension scores (CS) were subjected to a standard normal distribution transformation (nCS: normalized comprehension score). Two ANCOVAs were run on the dependent variables of FLI and GVAI, with the group as independent variable, to compare the SZ with their matched HCs and the BD with their matched HCs; nCS, gender, and age were used as covariates, and group × nCS interaction was also tested. Within the patient groups, ANCOVAs were run to test the effect of clinical variables. In SZ, the illness duration, total PANSS score, and AHRS score were added as covariates. In BD, the illness duration, HRSD, and HCL-20 scores were added to the model as covariates. Simple regressions between FLIs and GVAIs in each group were also tested and all statistical analyses were performed with JMP v10.0 Software (SAS Institute, Inc., Cary, NC). The level of significance was set at p b 0.05. 3. Results 3.1. SZ vs. HCs 3.1.1. FLIs The ANCOVA showed a significant group effect (p = 0.03*) and nCS effect (p = 0.002*) but no gender (p = 0.32), age (p = 0.11), or group × nCS interaction (p = 0.78) effects on the FLIs were seen. SZ presented a reduction in the leftward functional lateralization compared to HCs (Table 1). Regardless of group, FLIs were positively correlated with the nCS, meaning that the less leftward the FLIs were, the higher the nCS values were. Within the SZ, there was no effect of AHRS scores (p = 0.53), PANSS scores (p = 0.18), or illness duration (p = 0.91).

show a significant nCS effect (p = 0.0005*) on the GVAIs. GVAIs did not differ significantly between SZ and HCs (Table 1). Regardless of group, GVAIs were positively correlated with nCS, meaning that the less leftward the GVAIs were, the higher the nCS values were. Within the SZ, there was no effect of AHRS scores (p = 0.87), PANSS scores (p = 0.21), or illness duration (p = 0.97). 3.1.3. Correlations between FLAIs and GVAIs Positive and significant correlations between FLIs and GVAIs were found in both groups (patients with schizophrenia: R2 = 0.76, p b 10−3; healthy subjects: R2 = 0.68, p b 10−3). 3.2. BD vs. HCs 3.2.1. FLIs The ANCOVA showed no group (p = 0.64), nCS (p = 0.25), gender (p = 0.74), age (p = 0.57), or group × nCS interaction (p = 0.93) effects on FLIs. In addition, FLIs did not significantly differ between BD and HCs (Table 1). Within the BD group, there was no effect of HRSD scores (p = 0.34), HCL-20 scores (p = 0.45), or illness duration (p = 0.48). 3.2.2. GVAIs The ANCOVA showed no group (p = 0.53), nCS (p = 0.48), gender (p = 0.90), age (p = 0.80), or group × nCS interaction (p = 0.39) effects on the GVAIs. GVAIs did not differ significantly between BD and HCs (Table 1). Within the BD, there was no effect of HRSD scores (p = 0.24), HCL-20 scores (p = 0.45), or illness duration (p = 0.29). 3.2.3. Correlations between FLIs and GVAIs Positive and significant correlations between FLIs and GVAIs were found in both groups (patients with bipolar disorders: R2 = 0.84, p b 10−3; healthy subjects: R2 = 0.83, p b 10−3). 4. Discussion

3.1.2. GVAIs The ANCOVA showed no group (p = 0.27), gender (p = 0.08), age (p = 0.90), or group × nCS interaction (p = 0.44) effects but did

The present study showed that SZ presented a decreased leftward functional hemispheric lateralization for language compared with HCs

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whereas BD did not. Gray matter volume asymmetry in the language network was not reduced in patients with either schizophrenia or bipolar disorders compared to controls. A reduction in functional hemispheric lateralization for language in SZ is consistent with previous studies using other methods as well as various language tasks for distinct cerebral imaging analyses (whole brain or region of interest) (Sommer et al., 2003; Dollfus et al., 2005; Oertel et al., 2010; van Veelen et al., 2011; Sheng et al., 2013). Our results support the hypothesis of a reduction of leftward functional hemispheric lateralization for language in SZ compared to HCs, independently of task performance, severity of symptoms, age, and gender. The absence of reduced functional hemispheric lateralization for language in BD compared to HCs confirms our previous results (Alary et al., 2013b). Indeed, we have already found a decreased leftward functional hemispheric lateralization for language in SZ but not in BD. Although the present study involved some of the participants included in the previous work, more patients with each disorder were included in the current investigation. Furthermore, the HC group was carefully matched to both patient groups for gender, age, and education level. Few studies have investigated the gray matter volume of regions specifically involved in language networks in SZ, BD, and HCs. Ratnanather et al. (2013) reported a reduced gray matter volume in the planum temporale in SZ patients compared with HCs or BD. This finding is consistent with other studies that compared SZ with HCs and found that in SZ, the language structures were either decreased (Kasai et al., 2003; Iwashiro et al., 2012) or presented a reduced leftward asymmetry (Kawasaki et al., 2008; Oertel et al., 2010). To our knowledge, our study is the first to investigate gray matter volume asymmetries within an experimentally defined functional language network in both BD and SZ. The language network involved in the listening comprehension task implicates high-level semantic cognitive processes. Consequently, the results of the present study suggest that, in contrast to what was observed in the primary auditory cortex such as the planum temporale, gray matter volume asymmetry in a high-level semantic network is not modified in SZ (Kasai et al., 2003; Kawasaki et al., 2008; Oertel et al., 2010; Iwashiro et al., 2012; Ratnanather et al., 2013). The absence of any differences in terms of structural asymmetry between controls and the bipolar and schizophrenia patient groups can be usefully compared with the findings of Bora et al. (2012) who in a metaanalysis of VBM studies reported that differences in GM volume in schizophrenia and bipolar disorders were dependent on gender. Indeed, when gender-balanced samples of studies of schizophrenia were compared to the bipolar populations, asymmetries emerged: genderbalanced samples of studies of schizophrenia had GM decrease in the left dorsolateral prefrontal cortex and fronto-insular cortex/STG and the right dorsal ACC/dorsomedial frontal compared with controls. Bipolar disorders patients had GM deficits in the right ACC/medial frontal cortex, bilateral anterior insula/inferior frontal cortex and subgenual ACC/medial frontal cortex. However, GM differences between genderbalanced schizophrenia and bipolar disorder patients reached statistical significance only in the right dorsomedial frontal cortex and the left dorsolateral prefrontal cortex (smaller in schizophrenia). These findings provide a clue to the hemispheric organization of the human brain and its relevance to psychotic disorders. The present findings arise from a quite different paradigm, but are complementary in their implications for lateralization with respect to the faculty of language. They indicate that language lateralization is reduced in schizophrenia, but that this deficit is not accompanied by loss of gray matter in the structures necessary for comprehension. In bipolar disorders there are no deficits in either functional lateralization or gray matter in the relevant structures. Thus both studies yield evidence that in schizophrenia lateralization is impaired. While Bora et al. (2012) point to loss of gray matter as a possible mechanism of disturbance, the present study indicates that such loss, even in the structures directly involved in comprehension of stories is not necessary for the deficits either in comprehension or in

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asymmetry/lateralization of function. Moreover losses were reported by Bora et al. (2012) in the insula and the medial brain region (the ACC) that were not implicated in the functional network defined by the present protocol. Indeed, the structures identified in the present study comprise a functional network for language comprehension that apparently does not involve the insula or the ACC. Thus the findings may be interpreted as suggesting that a deficit in GM volume asymmetry does not underlie the core functional asymmetry deficit in patients with schizophrenia. This functional deficit, found only in schizophrenia, might be explained by other abnormalities, such as white matter impairment (Leroux et al., 2013) or changes in the shape or curvature of the temporal cortex (Plaze et al., 2011). Both FLIs and GVAIs were positively correlated with the nCS in SZ and their matched HCs. This result is consistent with previous studies in SZ in which interactions between cognitive task performances and BOLD variations were observed (Dollfus et al., 2005; Razafimandimby et al., 2011) and the fact that low performance can be responsible for hemisphere activation attenuation (Frith et al., 1995). The paradigm used in this study was passive and not demanding, and speech comprehension was irrepressible (Mazoyer et al., 1993), inducing activation of language areas in all cases, even in participants with low task performances. However, our results did not show any interaction between the group and the task performance (nCS) either for the FLIs or for the GVAIs. Moreover, in the SZ group as the matched HC group, FLIs were positively correlated with the nCS, meaning that the less leftward the FLIs were, the higher the nCS values were. This outcome indicates that the low performance could not explain the reduced lateralization in SZ. In this study, all groups presented a positive correlation between the structural and the functional asymmetries. As the gray matter structural asymmetry was estimated individually within the language functional network, strong correlations between FLAIs and GVAIs were expected and strengthened the validity of the method used. This result is also consistent with a study in healthy subjects in whom the degree to which language was left or right lateralized was positively correlated with the degree to which gray matter density was lateralized (Josse et al., 2009). Whether numerous studies reported reduced functional or structural brain asymmetry in patients with schizophrenia, few tested their relationships and observed less consistent results (Oertel et al., 2010; Alary et al., 2013a). For instance, anatomical and functional lateralization indices were significantly correlated for the planum temporale, but not for the Heschl gyrus. In a previous study, we found a positive correlation between GVAIs and FLIs in healthy subjects, while no such correlation was seen in patients with schizophrenia. This discrepancy could be related to the method, more refined in the present study. In the previous study, GVAIs were calculated in a mean functional map generated in healthy subjects while in the present study, GVAIs were calculated in the individual functional map from each patient and healthy control. Two strengths of the present study can be emphasized. First, functional hemispheric lateralization was determined with a robust index (FLIs) calculated in one specific language network. Second, the gray matter structural asymmetry was estimated individually within this same language functional network. Indeed, the FLIs allowed us to investigate the entire functional network involved in the language task, in contrast to most studies, which have used a region of interest approach. This latter method is threshold sensitive (Wilke and Lidzba, 2007) and thus can lead to varying results from one statistical threshold to another. In contrast, the approach used here allowed acquisition of more reproducible lateralization indices that are not subject to threshold effects, as demonstrated by Wilke and Lidzba (2007). In the same vein, the estimation of the structural asymmetry within the individual language functional network, based on the same method, also overcame the issue of inter-individual variability of activations, without being subject to statistical threshold effects. The study also has some limitations. First, SZ and BD could not be directly compared because they were not matched for age, gender, and

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level of education, variables known to be confounding factors. Second, both patient groups were stabilized with a low level of symptom severity; thus, the absence of correlations between brain asymmetries and clinical variables might not be representative of SZ and BD in general. Third, the laterality indices were calculated from a functional network involved in language processing. Therefore, the reduction in functional asymmetry in schizophrenia was observed only within the language network in question. It would be interesting to investigate another cognitive task involving a larger set of brain functions that involve the limbic structures (cingulate gyrus and parahippocampal gyrus) given the reported structural asymmetries of these structures in schizophrenia and bipolar disorder (Crow et al., 2013). In conclusion, our study demonstrated first that a reduced leftward functional hemispheric lateralization for language was observed only in SZ, not in BD or healthy controls. Second, this reduced leftward brain lateralization concerned only the functional network and not the gray matter volume within a specific language network. Finally, our results support the hypothesis that reduced leftward functional hemispheric lateralization for language could be a biomarker of schizophrenia. Role of funding source The French Health Ministry sponsored this study (Programme Hospitalier de Recherche Clinique (PHRC)) and allowed to pay the fees of promotion, insurance and logistical and administrative aspects: declarations to French drug Agency (ANMS) and ethics committee (CPP); elaboration of CRFs; data monitoring etc. The PHRC also supported the fees for anatomical and functional MRI, a research manager, full- or parttime hospitalizations, transports and catering for some patients and the compensation (150€ per scans) for all the subjects (patients and healthy subjects). The Association de Recherche pour la Schizophrenie (ARS) also provided financial support for the recruitment of an engineer for 2 months. Contributors Céline Royer carried out the statistical and MRI analyses and wrote the paper; Nicolas Delcroix supervised the data analyses, created the anatomical and functional sequences; Mathieu Alary provided the expertise in computing the functional laterality indexes; Annick Razafimandimby and Elise Leroux were involved in the preprocessing of MRI data; Perrine Brazo and Pascal Delamillieure recruited, evaluated the patients and acquired MRI data; Sonia Dollfus wrote the protocol and corrected the article, recruited and evaluated the patients, acquired MRI data and supervised all steps of the research (from acquirement to analyses). Conflict of interest All authors report no biomedical financial interests or potential conflicts of interest. Acknowledgements The authors are grateful to Tim Crow for having given us his opinion on our results in light of the literature. We also thank N. Tzourio-Mazoyer for having provided the functional language task, the French Ministry which sponsored this study (Programme Hospitalier de Recherche Clinique) and the Association de Recherche pour la Schizophrénie (ARS) which also provided financial support.

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Functional and structural brain asymmetries in patients with schizophrenia and bipolar disorders.

This study aimed to compare the functional and gray matter asymmetries in patients with schizophrenia (SZ), patients with bipolar disorders (BD), and ...
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