Alexithymia and regional gray matter alterations in schizophrenia
Research highlights
► Gray matter volume reductions in patients with schizophrenia were confirmed. ► An association between schizophrenia and alexithymia was revealed. ► Left supramarginal volume was negatively correlated with alexithymia in the patients.
Introduction
“Alexithymia” is a term derived from the Greek, meaning “lack (a)”, “word (lexis)”, and “emotion (thymos)”, and refers to deficits in recognizing, processing, and verbalizing emotions. The phenomenon was first described in patients with psychosomatic disorders (Sifneos, 1972) and was considered to represent difficulty discriminating between self emotional states and bodily sensations, as well as a shift in communicative styles, which are involved in the application of language (Taylor, 1984). A number of subsequent studies reported that alexithymia is found in other psychiatric disorders including eating disorders (Taylor et al., 1996, Bydlowski et al., 2005, Gilboa-Schechtman et al., 2006), dissociative disorders (Zlotnick et al., 1996, Elzinga et al., 2002, Sayar et al., 2005), posttraumatic stress disorder (Krystal et al., 1986, Alvarez and Shipko, 1991, Frewen et al., 2008), and pervasive developmental disorders (Fitzgerald and Molyneux, 2004, Tani et al., 2004, Szatmari et al., 2008). A relationship between alexithymia and schizophrenia has also been previously reported (Stanghellini and Ricca, 1995, Maggini and Raballo, 2004, Todarello et al., 2005, van’t Wout et al., 2007).
Meanwhile, impairments in various domains of social cognition have been highlighted in recent studies of schizophrenia. A number of studies have demonstrated impaired facial emotion processing (Mandal et al., 1998), theory of mind (ToM; Premack and Woodruff, 1978) abilities (Frith and Corcoran, 1996, Brüne, 2005), and empathy (Bora et al., 2008, Derntl et al., 2009) in schizophrenia.
Although alexithymia refers to a deficit in emotional self-awareness, rather than a deficit in the recognition of others’ emotions, Guttman and Laporte (2002) reported that alexithymia is inversely related to the ability of empathy. In addition, Dimaggio et al. (2008) noted that a representation of the self may act as a model for understanding the minds of others. That is, to understand what people are thinking about or how they feel, it may be crucial to understand and process our own emotions. As such, we hypothesize that impairments in social cognition and alexithymia may be co-existent and intercorrelated in schizophrenia.
Brain magnetic resonance imaging (MRI) studies have demonstrated multiregional brain alterations in patients with schizophrenia. Disproportionate gray matter (GM) reductions in a variety of prefrontal and temporal subregions have often been reported in previous structural MRI studies using manual volumetry (Shenton et al., 2001, Suzuki et al., 2005). Voxel-based morphometry (VBM; Ashburner and Friston, 2000) is a widely used, automated imaging-analysis method for exploring regional GM alterations throughout the whole brain. Recent meta-analyses of VBM studies in patients with schizophrenia have revealed widely consistent findings of GM reductions in bilateral superior temporal gyrus, bilateral medial prefrontal cortices, bilateral inferior frontal gyrus, right anterior cingulate gyrus, bilateral insula, bilateral parahippocampal gyrus, thalamus, and the left uncus/amygdala region (Honea et al., 2005, Ellison-Wright et al., 2008).
Moreover, recent neuroimaging studies on schizophrenia patients have gradually provided converging evidence elucidating the neural basis of impairments in social cognition. Previous studies in our laboratory have revealed that patients with schizophrenia exhibit impairments in emotion-intensity recognition (Namiki et al., 2007) and emotion-attribution tasks (Fujiwara et al., 2007, Yamada et al., 2007), which are correlated with volume reductions in the amygdala and medial frontal lobes, respectively. As for ToM and empathy impairments in schizophrenia, structural and functional abnormalities have been reported in the left temporoparietal junction (TPJ), temporal pole, medial prefrontal cortex, and left ventrolateral prefrontal cortex (Hirao et al., 2008, Benedetti et al., 2009).
While the neural basis of alexithymia remains a subject of ongoing investigation, previous neuroimaging studies have suggested the importance of the anterior cingulate cortex (ACC), orbitofrontal cortex, dorsolateral prefrontal cortex, and insula in alexithymia in healthy subjects (Kano et al., 2003, Moriguchi et al., 2007b, Borsci et al., 2009). However, the relationship between brain alterations and alexithymia in schizophrenia remains unclear, and so far there have been no studies exploring such a relationship in the whole brain in schizophrenia.
Thus, in this study, we applied the Japanese version of the 20-item Toronto Alexithymia Scale (TAS-20; Bagby et al., 1994a, Bagby et al., 1994b, Moriguchi et al., 2007a) and VBM to elucidate the association between alexithymia and regional GM alterations in patients with schizophrenia. With its relatively high reliability and validity, the TAS-20 is widely used for measuring alexithymia (Moriguchi et al., 2007a), and was used to assess alexithymia in previous studies on patients with schizophrenia (Maggini and Raballo, 2004, Todarello et al., 2005).
We developed three hypotheses for this study: (1) that alexithymia would be detected in patients with schizophrenia, possibly exhibiting a specific pattern; (2) that GM volume reductions would be exhibited in schizophrenia, and specific regional GM alterations would be related to alexithymia in schizophrenia, which reflect the components of alexithymia; and (3) that the latter regions would also overlap with the cortical and subcortical structures that are critical for social cognition.
Section snippets
Participants
The schizophrenia group comprised 21 patients (14 men and seven women, all right-handed) who were referred to the Department of Psychiatry, Kyoto University Hospital. Each patient fulfilled the criteria for schizophrenia based on the Structural Clinical Interview for DSM-IV (SCID). Psychopathology was assessed using the Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987). All patients were receiving antipsychotic medication (typical [n = 2], atypical [n = 14], typical and atypical [n =
Basic cognitive tasks
The estimated VIQ (t = 3.95, P < 0.001) and PIQ (t = 2.92, P = 0.006) were significantly lower in patients with schizophrenia than in controls. However, there was no significant difference in predicted IQ between patients with schizophrenia and controls (Table 1).
TAS-20 scores
TAS-20 results are shown in Fig. 1 and Table 2.
An independent sample t-test revealed that TAS-20 total scores were significantly higher in the patient group than in the control group (t = −5.6, P < 0.001).
There were no significant correlations
Discussion
To our knowledge, this is the first study to investigate the relationship between alexithymia and brain volume in patients with schizophrenia using VBM.
Our results revealed an association between schizophrenia and alexithymia, consistent with previous studies on schizophrenia using TAS-20 (Maggini and Raballo, 2004, Todarello et al., 2005) and other scales of alexithymia (Stanghellini and Ricca, 1995, van’t Wout et al., 2007). Our results, showing highly significant group differences for DIF
Acknowledgments
This work was supported by a grant-in-aid for scientific research from the Japan Society for the Promotion of Science and the Ministry of Education, Culture, Sports, Science and Technology, Japan [21890119 to Jun Miyata; 20691401 to Toshiya Murai]; a grant from the Ministry of Health, Labour and Welfare, Japan [20E-3 to Toshiya Murai]; a research grant from the Research Group for Schizophrenia sponsored by Astellas Pharma Inc., and a research grant from Mitsubishi Pharma Research Foundation.
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