Creativity and positive symptoms in schizophrenia revisited: Structural connectivity analysis with diffusion tensor imaging

https://doi.org/10.1016/j.schres.2015.03.009Get rights and content

Abstract

Both creativity and schizotypy are suggested to be manifestations of the hyperactivation of unusual or remote concepts/words. However, the results of studies on creativity in schizophrenia are diverse, possibly due to the multifaceted aspects of creativity and difficulties of differentiating adaptive creativity from pathological schizotypy/positive symptoms. To date, there have been no detailed studies comprehensively investigating creativity, positive symptoms including delusions, and their neural bases in schizophrenia. In this study, we investigated 43 schizophrenia and 36 healthy participants using diffusion tensor imaging. We used idea, design, and verbal (semantic and phonological) fluency tests as creativity scores and Peters Delusions Inventory as delusion scores. Subsequently, we investigated group differences in every psychological score, correlations between fluency and delusions, and relationships between these scores and white matter integrity using tract-based spatial statistics (TBSS). In schizophrenia, idea and verbal fluency were significantly lower in general, and delusion score was higher than in healthy controls, whereas there were no group differences in design fluency. We also found positive correlation between phonological fluency and delusions in schizophrenia. By correlation analyses using TBSS, we found that the anterior part of corpus callosum was the substantially overlapped area, negatively correlated with both phonological fluency and delusion severity. Our results suggest that the anterior interhemispheric dysconnectivity might be associated with executive dysfunction, and disinhibited automatic spreading activation in the semantic network was manifested as uncontrollable phonological fluency or delusions. This dysconnectivity could be one possible neural basis that differentiates pathological positive symptoms from adaptive creativity.

Introduction

Creativity has long been thought as the ability to produce original, novel, flexible, and useful ideas that are free from established mental habit. One of the most commonly used definitions is “the production of effective novelty” (Mumford, 2003). A number of factors are thought to be related to creativity, such as divergent thinking (Guilford, 1959), openness (Dollinger et al., 2004), handedness (Shobe et al., 2009), language (Leonhard and Brugger, 1998), problem solving, adaptability, self-expression, quality of life (Runco, 2004), artistry (Bhattacharya and Petsche, 2002, Bhattacharya and Petsche, 2005), magical ideation (Badzakova-Trajkov et al., 2011), and schizotypy (Fisher et al., 2004).

Both creativity and schizotypy are suggested to be manifestations of the hyperactivation of unusual or remote concepts/words (Mohr et al., 2001). Therefore, relationships between creativity and schizophrenia-spectrum disorder have been widely investigated (Sass, 2000, Nelson and Rawlings, 2010). Indeed, a study reported that schizophrenia patients tended to engage in artistic occupation (Kyaga et al., 2011). However the results of studies on creativity in schizophrenia are varied. Some studies reported enhanced mental imagery manipulation in schizophrenia using jigsaw puzzle task (Benson and Park, 2013), whereas other studies reported lower figural creativity using the Berlin Intelligence Structure Test (Jaracz et al., 2012) or lower creativity in general using design, idea, and word fluency tests (Nemoto et al., 2007) in schizophrenia. One possible reason for these inconsistencies may be found in the differences in definition and measurement methods of creativity. Furthermore, Tsakanikos et al. reported that increased positive schizotypy or positive symptoms had relationships with increased creativity, whereas negative schizotypy or negative symptoms could be related to reduced creativity (Tsakanikos and Claridge, 2005). Thus, the clinical background of patients should also be taken into account in respect to such inconsistencies.

In previous literature investigating the semantic priming effect, it has been suggested that enhanced automatic spreading activation in semantic networks is associated with creativity (Tsakanikos and Claridge, 2005), and might underlie some of the positive symptoms (Spitzer, 1997) such as thought disorder (Kreher et al., 2008), hallucination (Lindamer and Whitman, 1997, Kerns et al., 1999), or delusion (Debruille et al., 2007) in schizophrenia. Thus, it is reasonable to ask the following questions: what is the difference between creativity and positive symptoms, or why could hyperactivation result in innovative output in one case, but in psychotic symptoms in another? Fisher et al., in dealing with these questions, suggested that frontal lobe functions, i.e., executive functions such as monitoring, controlling, or inhibiting ability, play pivotal roles in the use of semantic information and differentiate creativity from psychopathology (Fisher et al., 2013).

Therefore, in this study, we aimed to examine creativity in schizophrenia patients with multiple creativity measures with and without semantic contents, and to investigate its impact on psychopathology, especially on positive symptoms. We predicted that overall creativity performance in schizophrenia might increase or decrease depending on the proportion of positive and negative symptoms, and that some creativity measures would positively correlate with positive symptoms. Furthermore, we hypothesized that this correlation between creativity and pathological, positive symptoms would be underpinned by the pathology of the frontal lobe structure. One of the influential hypotheses of schizophrenia, “the disconnection hypothesis” (Friston, 1998), assumes that dysconnectivity among multiple neural systems might underlie some symptoms of schizophrenia, mainly positive symptoms. We therefore utilized diffusion tensor imaging (DTI) to investigate the structural connectivity, and examined its relation with creativity and psychopathology.

Section snippets

Participants

Forty-three patients with schizophrenia (22 men and 21 women, age = 37.37 ± 8.66) were recruited. Each patient fulfilled the criteria for schizophrenia based on the Structural Clinical Interview for DSM-IV Axis I Disorders (SCID) Patients Edition, Version 2.0. None of the patients were comorbid with other mental disorders. Predicted IQ was measured using the Japanese Version of the National Adult Reading Test (JART) short form (Matsuoka et al., 2006, Matsuoka and Kim, 2007), which is thought to

Scores of fluency tasks and PDI

Demographic and clinical data are shown in Table 1a. Many patients had mild symptom severity. The scores of fluency tasks and PDI are shown in Table 1b. Inter-rater reliabilities of scoring fluency tasks between two examiners, “SS” and “MK”, were P = .98 in Idea Td, .96 in Idea Tm, .95 in Idea Ti, 1.00 in Design Td, 1.00 in Design Tm, and 1.00 in Design Ti. An independent sample t-test revealed that Idea Tm, Idea Ti, Verbal C, and Verbal L were significantly lower and PDI was higher in

Discussion

Using comprehensive creativity scales and structural connectivity with DTI, we found decreased idea and verbal fluency in general, but retained design fluency in schizophrenia. In the schizophrenia group, phonological fluency was positively correlated with delusion severity. DTI analyses revealed correlation between frontal white matter integrity and phonological fluency, and between widespread white matter region and delusion severity in schizophrenia. These two results showed substantial

Role of funding source

This work was supported by grants-in-aid for scientific research A (24243061), B (23390290), S (22220003), and on innovative areas (23118004, 23120009), from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT), and Grants-in-Aid for Young Scientists A (23680045), B (23791329) from the Japan Society for the Promotion of Science. A part of this study is the result of Development of BMI Technologies for Clinical Application carried out under the Strategic Research

Contributors

Shuraku Son designed the study and wrote the protocol, and also managed the literature searches and analyses and wrote the first draft of the manuscript. Shuraku Son, Manabu Kubota, and Jun Miyata undertook the analysis and interpretation of clinical and psychological data. Shuraku Son performed data processing and statistical analyses, under technical supervision by Manabu Kubota, Jun Miyata, Toshihiko Aso, Shin-ichi Urayama, Hidenao Fukuyama, Toshiya Murai, and Hidehiko Takahashi. All authors

Conflict of interest

All authors declare that they have no conflicts of interest in this study.

Acknowledgment

The authors wish to extend their gratitude to Kimito Hirose, Kousuke Tsurumi, Masanori Isobe, Miki Ono, Naoto Yokoyama, and Yasuo Mori for their assistance in data acquisition and are especially thankful to the patients and volunteers for participating in the study.

References (50)

  • R.S.E. Keefe et al.

    The brief assessment of cognition in schizophrenia: reliability, sensitivity, and comparison with a standard neurocognitive battery

    Schizophr. Res.

    (2004)
  • J.G. Kerns et al.

    Word production in schizophrenia and its relationship to positive symptoms

    Psychiatry Res.

    (1999)
  • D. Mamah et al.

    Anterior thalamic radiation integrity in schizophrenia: a diffusion-tensor imaging study

    Psychiatry Res.

    (2010)
  • T. Nemoto et al.

    Contribution of divergent thinking to community functioning in schizophrenia

    Prog. Neuropsychopharmacol. Biol. Psychiatry

    (2007)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • E.R. Shobe et al.

    Influence of handedness and bilateral eye movements on creativity

    Brain Cogn.

    (2009)
  • S.M. Smith et al.

    Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference

    NeuroImage

    (2009)
  • C. Sumiyoshi et al.

    Disorganization of semantic memory underlies alogia in schizophrenia: an analysis of verbal fluency performance in Japanese subjects

    Schizophr. Res.

    (2005)
  • E. Tsakanikos et al.

    More words, less words: verbal fluency as a function of ‘positive’ and ‘negative’ schizotypy

    Personal. Individ. Differ.

    (2005)
  • H.A. Allen et al.

    Negative features, retrieval processes and verbal fluency in schizophrenia

    Br. J. Psychiatry

    (1993)
  • T.L. Benson et al.

    Exceptional visuospatial imagery in schizophrenia; implications for madness and creativity

    Front. Hum. Neurosci.

    (2013)
  • J. Bhattacharya et al.

    Drawing on mind's canvas: differences in cortical integration patterns between artists and non-artists

    Hum. Brain Mapp.

    (2005)
  • E.R. Cardillo et al.

    Left inferior prefrontal cortex activity reflects inhibitory rather than facilitatory priming

    J. Cogn. Neurosci.

    (2004)
  • S.J. Dollinger et al.

    Creativity and openness: further validation of two creative product measures

    Creat. Res. J.

    (2004)
  • T.J. Edwards et al.

    Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes

    Brain

    (2014)
  • Cited by (17)

    • Aging and Creativity

      2021, Aging and Creativity
    • Neurocognitive, social cognitive, and clinical predictors of creativity in schizophrenia

      2020, Journal of Psychiatric Research
      Citation Excerpt :

      However, studies carried out with people with schizophrenia have not found very consistent results (Abraham et al., 2007; Jaracz et al., 2012; Son et al., 2015). For example, Son et al. (2015) did not find any significant correlation between creativity and positive symptoms. Abraham et al. (2007) found thought disorder to be significantly related to lower scores in some creativity indexes.

    • Creativity and psychiatric illness: A functional perspective beyond chaos

      2018, Progress in Neuro-Psychopharmacology and Biological Psychiatry
      Citation Excerpt :

      Even if this link is reported in several studies, others failed to do so (Kyaga et al., 2011). These contrasting data could be explained by choosing different measurement methods evaluating creativity aspects, different creativity definitions and different clinical backgrounds of the patients (Tsakanikos and Claridge, 2005; Son et al., 2015). The term “Schizotipy” is used to denote schizophrenia-like features (Ando et al., 2014).

    • Is the link between autistic traits and ability to succeed in science independent of other psychopathological dimensions?

      2016, Revue Europeenne de Psychologie Appliquee
      Citation Excerpt :

      In agreement with this, two other research groups showed that schizophrenia patients and individuals with higher creativity displayed comparable brain activities, characterized by a reduced suppression of prefrontal cortex during a working memory task (Whitfield-Gabrieli et al., 2009; Takeuchi et al., 2012). More recently, another evidence of a functional link between creativity and schizotypy was brought by a report describing that disrupted inter- and intra-hemispheric connections projecting to frontal areas underlie positive symptoms or creativity in schizophrenia patients (Son et al., 2015). Another link between personality and scientific abilities was brought to light by research groups studying the psychological profile of high school students.

    View all citing articles on Scopus
    View full text