Elsevier

NeuroImage

Volume 102, Part 2, 15 November 2014, Pages 474-483
NeuroImage

Association of creative achievement with cognitive flexibility by a combined voxel-based morphometry and resting-state functional connectivity study

https://doi.org/10.1016/j.neuroimage.2014.08.008Get rights and content

Highlights

  • Real-life creativity is assessed using creative achievement questionnaire.

  • Individual with high creative achievement (CA) displays more cognitive flexibility.

  • CA is related to GMV of brain regions involved in deliberate creative processing.

  • CA is inversely correlated to dACC–mSFG connectivity within the salience network.

  • Cognitive flexibility mediates the association between dACC–mSFG connectivity and CA.

Abstract

Although researchers generally concur that creativity involves the production of novel and useful products, the neural basis of creativity remains elusive due to the complexity of the cognitive processes involved. Recent studies have shown that highly creative individuals displayed more cognitive flexibility. However, direct evidence supporting the relationship between creativity and cognitive flexibility has rarely been investigated using both structural and functional neuroimaging techniques. We used a combined voxel-based morphometry and resting-state functional connectivity (rsFC) analysis to investigate the relationship between individual creativity ability assessed by the creative achievement questionnaire (CAQ), and regional gray matter volume (GMV), as well as intrinsic functional connectivity. Results showed that CAQ scores negatively correlated with GMV in the rostral anterior cingulate cortex (ACC) and the bilateral dorsal ACC (dACC) extending to supplementary motor area, but positively correlated with GMV in the bilateral superior frontal gyrus and ventral medial prefrontal cortex (vmPFC). Further functional connectivity analysis revealed that higher creative achievement was inversely associated with the strength of rsFC between the dACC and medial superior frontal gyrus (mSFG), right middle frontal gyrus, and left orbito-frontal insula. Moreover, the association between the dACC–mSFG connectivity and CAQ scores was mediated by cognitive flexibility, assessed by a task-switching paradigm. These findings indicate that individual differences in creative achievement are associated with both brain structure and corresponding intrinsic functional connectivity involved in cognitive flexibility and deliberate creative processing. Furthermore, dACC–mSFG connectivity may affect creative achievement through its impact on cognitive flexibility.

Introduction

Creativity has been commonly viewed as the cornerstone of human civilization. Although researchers generally concur that creativity involves both original and useful behaviors or products (Runco and Jaeger, 2012, Stein, 1953, Sternberg and Lubart, 1996), the neurocognitive mechanisms remain elusive, due largely to the complex cognitive processes likely involved in creative cognition (Chávez-Eakle et al., 2007, Jung et al., 2010b). A large body of research has supported the notion that creative thought is closely linked to spontaneously occurring cognition, such as lower working memory demands (Takeuchi et al., 2011a), defocused attention (Vartanian, 2009, Wegbreit et al., 2012), and mind wandering (Baird et al., 2012). However, recent studies indicate that more deliberate processing, characterized by strong cognitive control (Groborz and Necka, 2003), high working memory capacity (De Dreu et al., 2012), and higher motor planning (Aziz-Zadeh et al., 2013) plays a critical role in the performance of creative tasks. Regarding deliberate creativity, several researchers have speculated that cognitive flexibility, which reflects the adaptability of thought and behavior (Collins and Koechlin, 2012), could facilitate a shift of thought in the face of environmental change, leading to generation of innovative ideas and the promotion of new discoveries (Barbey et al., 2013, De Dreu et al., 2011). Dietrich (2004) notes that creativity is the epitome of cognitive flexibility; however, a direct evidence supporting the relationship between creativity and cognitive flexibility has rarely been investigated using both structural and functional neuroimaging techniques.

In describing the neurocognitive basis of creativity, many studies have focused on verbal creativity (e.g. divergent thinking tasks, remote associates test). Previous brain imaging studies support the notion of spontaneous creativity that emphasizes creative insight, and that original ideas rely on automatic processing and a modulation of bottom-up attention (Fink et al., 2010, Jung-Beeman et al., 2004). However, some studies of visual creativity (e.g. product design, visuospatial creativity problem) emphasize the central role of prefrontal cortex contribution to cognitive performance required in creative tasks, such as working memory, sustained attention, cognitive flexibility, and goal-directed planning (Aziz-Zadeh et al., 2013, Kowatari et al., 2009). A study of musical improvisation found increased activity in prefrontal cortices, including the inferior frontal gyrus, ACC, and supplementary motor cortex (SMA), supporting the working memory and executive control aspects of cognition (de Manzano and Ullen, 2012). Thus, it appears that the different tasks used by creative researchers yield different results when compared across various divergent thinking tasks or insight problems (Arden et al., 2010).

In reality, creativity does not appear to depend on a single cognitive process or brain region (Arden et al., 2010, Dietrich and Kanso, 2010). Creative acts depend on a distributed neural network and multiple cognitive processes (Jung et al., 2013). During the past decade, a given cognitive process (e.g., insight, divergent thinking) has been demonstrated to be one of many components that constitute creative thinking. Unfortunately, studies carried out to date yield inconsistent results, and authoritative reviews on the neuroscience of creativity (Arden et al., 2010, Dietrich and Kanso, 2010) have criticized that the field is fragmented, with poor theoretical concepts. This problem may be approached by using ecologically valid measurements that contain multiple domains of ability, and involve the production of useful and novel products (Arden et al., 2010, Sawyer, 2011), such as art, problem solving, invention, cooking etc. To our knowledge, real-life creativity measures such as creative achievement, which is defined as the sum of creative products generated by an individual in the course of his or her lifetime, involves long-term creative behaviors and reflects the best current measure of inter-individual differences of creative ability (Carson et al., 2005). In short, a measure involving comprehensive abilities may help us to better understand the nature of creativity.

Recent behavioral studies have identified that people with high creative achievements display more flexible cognitive control (De Dreu et al., 2011, Zabelina and Robinson, 2010), broadly defined as the capacity to adjust one's thinking in the face of environmental change as well as the ability to overcome obvious thinking and adapt to new situations (Moore and Malinowski, 2009). One possible interpretation is that greater cognitive control is of benefit for creative actions when automatic processes fail (Miller and Cohen, 2001, Zabelina and Robinson, 2010). Indeed, creative products are achieved through some combination of cognitive flexibility and persistence (De Dreu et al., 2011). From this perspective, flexible cognitive performance relies on the activation of brain regions engaged in cognitive control, such as the ACC, medial frontal cortex, and dorsolateral prefrontal cortex (Clare Kelly et al., 2006, Kerns et al., 2004, Ridderinkhof et al., 2004). Additionally, psychological, functional imaging, and genetic studies have reported a positive relationship between individual creativity and dopaminergic systems (Chermahini and Hommel, 2010, Mayseless et al., 2013, Takeuchi et al., 2010a). Dopaminergic system includes the prefrontal cortex, with mesolimbic areas contributing to creativity through its effect on goal-directedness, novelty-seeking, or creative drive (Flaherty, 2005).

With regard to the inter-individual differences of creativity, previous studies have focused on brain structure, revealing a large-scale network of brain regions involved in creative thinking, including subcortical regions (Takeuchi et al., 2010a), the corpus callosum (Takeuchi et al., 2010b), inferior frontal (Jung et al., 2010a), bilateral fronto-parietal regions (Takeuchi et al., 2011b), and posterior parietal and occipital regions (Fink et al., 2013). While altered brain structure is interpreted as indicative of creative abilities, such as divergent thinking, openness, or vivid imagination, none of these studies have been independently replicated. Moreover, robust evidence has shown that functional networks associated with the brain's resting state are highly predicted by structural connections in the same cohort of participants (Bullmore and Sporns, 2009). Recent studies also suggest that gray matter volume (GMV) changes in brain areas are commonly accompanied by intrinsic functional network alterations in these regions (Gili et al., 2011, Li et al., 2012). In light of these findings, we predicted that intrinsic functional networks, dependent upon structural brain features, would be correlated with a variation in creative achievement. Considering that real-life creative behaviors are typically characterized by cognitive flexibility and cognitive control, two main brain networks, including the salience network (SN) and the fronto-parietal (FP) network were focused on. According to the recent model, the SN is centered on fronto-insular and dorsal anterior cingulate cortical (dACC) regions, which combine to facilitate the access to attention and working memory by switching between other large-scale neural networks (Menon and Uddin, 2010). Simultaneously, the SN appears to play an important role in the frontostriatal dopaminergic system in mediating motivated behaviors (Cole et al., 2013) and flexibility cognitive control, likely relevant for individual creative achievement. In addition, the FP component includes regions including bilateral DLPFC and lateral parietal cortices, the combined activation of which are involved in sustained attention and working memory tasks in processes of cognitive control (Seeley et al., 2007). Neuroimaging studies of creativity also reveal that creative processes induced frontoparietal activation, which were thought to be involved in analogical reasoning (Green et al., 2012), goal-directed planning (Aziz-Zadeh et al., 2013), and idea evaluation (Ellamil et al., 2012).

In the current study, the participants underwent MRI scans and out-of-scanner psychological tests that contained creative achievement assessment, a task-switching paradigm, and intelligence testing. First, we assessed the relationship between GMV and individual creative achievement. Based on previous works showing an association between creativity and distributed brain areas involved in the cognitive control processing regions and dopamine systems (Aziz-Zadeh et al., 2013, Kowatari et al., 2009, Takeuchi et al., 2010a), we hypothesized that GMV in the regions related to cognitive control processing such as ACC, and dopaminergic systems such as the PFC, and midbrain structures, would be associated with individual real-life creative performance measured by the creative achievement questionnaire (CAQ). Additionally, during task-free conditions, better performance on divergent thinking task is correlated with greater resting-state functional connectivity (rsFC) between the posterior cingulate cortex and medial prefrontal nodes of the default mode network (DMN) (Takeuchi et al., 2012), which is anticorrelated with the SN included ACC and bilateral frontoinsular cortex (Sridharan et al., 2008). Thus, we expected that increased regional functional connectivity in the SN would be negatively associated with creative achievement. Finally, we performed exploratory mediation analyses to examine whether cognitive flexibility could account for the relationship between creative achievement and regional functional connectivity in the SN.

Section snippets

Subjects

This study is part of our ongoing project to explore the association between brain imaging, creativity, and mental health. 385 healthy volunteers participated in this study. 19 participants were excluded due to missing data (9 participants including 5 people with large motion artifacts and 4 people with porencephaly or hydrocephalus) and lack of behavioral data (10 participants). Thus the final sample was comprised of 366 participants (165 males; mean age = 20, SD = 1.33 years). Most of the

Behavioral data

Table 1 shows the descriptive statistics of the demographic and psychological characteristics of all participants. CAQ scores showed no significant gender differences. Correlation analysis was conducted on 164 participants (valid samples) and showed CAQ scores to be negatively correlated with the RT of task switching (r = 0.23, p < 0.01), the difference of RT between switch trials and repetition trials. This revealed that subjects with high creative achievement displayed more cognitive flexibility

Discussion

This study examined the relationship between the inter-individual creative achievement and regional GMV as well as intrinsic functional connectivity. Consistent with our expectations, the findings supported our hypothesis and extended previous research in three ways: (a) by showing that individual creative ability was associated with altered GMV involved in cognitive control regions; (b) by performing functional connectivity analysis and identifying that higher creative achievement was

Acknowledgments

The authors would like to thank the participants, the testers for the ongoing project, and all our other colleagues for their support. We would like to thank Rex Jung for his assistance with language. We also thank the anonymous reviewers for their insightful comments and criticisms. This research was supported by the National Natural Science Foundation of China (31170983; 31271087).

Conflict of interest

The authors declare no competing interests.

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