Introduction

Creativity refers to the ability of an individual to produce novel and practical products or points of view [1]. Such ability is known to serves as pillars of society, affecting all aspects of human life [2,3]. The progress and innovation of human society rely on the ability of individuals to step out of the box and breathe new life to things [3]. Hence, creativity is essential to the development of human civilization and plays a crucial role in cultural life. Modern creativity research is attributed mainly to Joy Paul Guilford in 1950. Guilford indicated that creative thinking is the concrete manifestation of individual creativity, and that divergent and convergent thinking together constitute complete creative thinking, the core of which is divergent thinking [4]. Divergent thinking refers to the ability of an individual to develop several solutions to a highly complex open-ended problem [5]. This component of creative thinking has attracted considerable attention because it characterizes a technique for pushing difficult problems into the realm of empirical science [3]. This focus on divergent thinking has led to the development of several standardized psychometric instruments of creativity. The Torrance Test of Creative Thinking (TTCT) [6] is a well-established creativity test for measuring creative thinking focusing on divergent thinking. Many experimental paradigms, developed from TTCT, have been applied in laboratory-based research on creativity. With the emergence of cognitive neuroscience, new research techniques, including high temporal resolution brain electrophysiology such as electroencephalograph (EEG), event-related potential (ERP) and high spatial resolution neuroimage techniques such as diffusion tensor imaging (DTI) and functional magnetic resonance imaging (fMRI) have been applied in cognitive psychology. These approaches, along with behavioral assessment tools on creativity, can help researchers explore the neural mechanism of the creative thinking process.

Efforts have focused on creativity-related functional brain areas [7-15]. In their review, Fink and Benedek (2012) argued that in focusing on one measure of brain activation (i.e., alpha power in the EEG), task- or event-related increases in alpha synchronization during creative ideation were often seen at the prefrontal and parietal and occipital sites [16,17]. For instance, Fink and Neubauer (2006) conducted an EEG study on creativity, and aimed to explore the following two tasks derived from TTCT: a) an unusual situation in that requires explanation, such as “a light in the darkness”; and b) a utopian situation that will never actually happen, such as “Imagine, there were a creeping plant rising up to the sky. What would you await at the end of this plant?” The participants of both tasks were asked to imagine themselves in the given situations and to visualize possible causes and outcomes. The result of the study reflected a frontal alpha synchronization during the performance of the tasks, indicating that the generation of novel ideas involves an top-down inhibition function in the prefrontal cortex and a right parietal alpha synchronization involved in vivid imaginative abilities during creative ideation [7]. In another review, Dietrich and Kanso (2010) suggested that in focusing on the functional aspects of brain activity, such as fMRI, PET, and NIRS, and on the well-established creative thinking process (or more generally on divergent thinking), difficulties in identifying replicable brain correlates underlying creativity were apparent [3]. Despite the diversity of the functional activation patterns among these neuroimaging studies, the activation of prefrontal regions was consistently reported [3]. The authors argued that the data permit the conclusion that the prefrontal cortex has a key role in divergent thinking. Beyond this rather general statement, however, a more specific premise is not possible [3].

Aside from the task-related functional research on creativity mentioned above, a few recent studies have focused on the cerebral structural basis of creativity and on the inter-individual differences in creativity [14,16,18-22]. Overall, similar to the diversity of the creativity-related functional brain areas, the creativity-related brain structures were also scattered and diffused in different studies. For example, Jung et al. (2010) observed a relationship between creativity and cortical thickness in several brain regions including the lingual gyrus, the right posterior cingulate, the left lateral orbitofrontal and the right angular gyrus [14]. In terms of white matter microstructure, creative performance was found to be positively correlated with white matter integrity, as assessed by fractional anisotropy (FA)，in the left superior frontal gyrus [18]. Takeuchi et al. (2010a) reported a positive correlations between regional GMV and individual creativity in several regions known to be associated with the dopaminergic system, such as the right dorsolateral prefrontal cortex (DLPFC), the bilateral striata, the substantia nigra, tegmental ventral area and periaqueductal [20]. Another study conducted by Takeuchi et al. (2010b) suggested that individual creativity is remarkably positively correlated with FA in the bilateral prefrontal cortices, the body of the corpus callosum, the bilateral basal ganglia, the bilateral temporo-parietal junction and in the right inferior parietal lobule [19]. Fink et al. (2013) reported that verbal creativity was significantly and positively associated with gray matter density (GMD) in clusters within the right cuneus and the right precuneus [16]. The inconsistency of these studies may be primarily due to the broad diversity in measuring creativity as well as to the diversity of experimental procedures and methodologies used in this field of research. For instance, the discrepancies between Takeuchi et al. (2010a) and Jung et al. (2010) might be due to the neuroimaging method used (GMV with VBM in Takeuchi et al. 2010a vs. cortical thickness in Jung et al2010), but also to the psychometric measures that they used to assess ‘‘creativity’’ (verbal divergent thinking tasks were used to measure creativity in Takeuchi et al. 2010a vs. both verbal and figural divergent thinking tasks in Jung et al. 2010). The discrepancies between Takeuchi et al. (2010a) and Fink et al. (2013) might be due to the difference in the index of brain structures that were measured [GMV in Takeuchi et al. (2010a) vs. GMD in Fink et al. (2013)]. In addition, in closely examining these results, we could see that all these studies, except Fink et al. (2013), reported that prefrontal brain areas correlated with creativity.

Creativity is not a prime example for a unitary or homogeneous construct [3,17]; hence, neuroscientists have faced many challenges to decompose the multifaceted construct of creativity into smaller and more definable units (i.e., verbal creativity, figural creativity, and art creativity), and to specifically relate these subcomponents of creativity to both the structural and functional parameters of the brain. Several studies challenged this issue [e.g., Takeuchi et al. (2010a) and Fink et al. (2013)]. In addition, one study [22], aimed at examining the relationships between brain connectivity and visuospatial divergent thinking (measured by the figural TTCT) chose the corpus callosum as a region of interest (ROI) because of the postulate that inter-hemispheric connectivity is critical for divergent thinking. The authors found that the creative visuospatial performance is inversely related to the size of the corpus callosum. They suggested that decreased callosal connectivity enhances hemispheric specialization. In particular, the callosal sectioning prevented the visuospatial analysis performed by the right hemisphere from reaching the verbal left hemisphere [22]. As a supplement for the neural anatomy of creative visuospatial performance, Gansler et al. (2011) applied a statistics analysis of ROIs to explore the gray matter structure associated with creative visuospatial performance (also assessed by the figural TTCT) the authors found that creative visuospatial performance is associated with GMV in the right parietal lobe, which is believed to be important in visuospatial processing [21]. The study further reported that visuospatial divergent thinking requires some specialized cerebral functions (visuospatial imagery and skills) that may be mediated by the right parietal lobe.

In this study, we focused on verbal creativity measured by the verbal TTCT and on the neural correlates of verbal creativity to complement the structural brain research on definable units of creativity. The verbal TTCT comprises seven verbal tasks or items. The tasks applied in Takeuchi et al. (2010a) and Fink et al. (2013) are only a part [three tasks in Takeuchi et al. (2010a) and one task in Fink et al. (2013)] developed from the verbal TTCT. We thought that using all seven tasks from the verbal TTCT might provide a higher validity because in the same reliability, validity increases with the increase in the items. In terms of the index of brain structures, GMV, rather than GMD, was obtained with an optimal voxel-based morphometry (VBM), which is an automated technique for assessing structural changes in the brain. (see Images preprocessing for VBM, Method in details). One purpose of our study was to verify whether these brain correlates underlying verbal creative thinking in Takeuchi et al. (2010a) and Fink et al. (2013) can be stably manifested in our replicable experiment. Conversely, we wondered that if healthy participants with greater visuospatial creativity have larger GMVs in the right parietal lobe, then people with different verbal creative ability may also demonstrate differences in the cortical regions involving language cognition and divergent thinking. Specifically, the bilateral prefrontal cortices might be the cortical areas where these differences may likely be manifested. As mentioned above, the prefrontal cortex is known to play an important role in creative thinking. A recent study associated the left inferior frontal gyrus (IFG) activation with novelty-based representations originating from the development and selection of semantic relatedness [23]. In addition, language production and comprehension are known to be mediated by Broca’s area (BA44 and BA45), which is a part of the left IFG [24-26]. Based on the idea that the volume of cortical tissue devoted to a certain function influences the quality of a person’s ability to perform that function, verbal creative performance was proposed to be associated with cerebral (GMVs) or/and white matter volumes (WMVs) in the brain regions that are believed to be important in verbal processing and divergent thinking, such as Broca’s area or the left IFG and bilateral prefrontal cortices.

Methods

Results

Correlation between GMVs and verbal creativity

After control for age, gender, general intelligence, and total gray matter volume in the multiple regression analysis, the correlation of GMVs with verbal creative thinking measured by verbal TTCT was determined (Table 2). As shown in Table 2, significantly positive correlation was found between the verbal TTCT score and the left IFG, pars triangularis (BA45: x = -50, y = 31, z = 15; see also Figure 1A), and the right IFG (x =60, y = 10, z = 17; see also Figure 1C). All voxels survived at cluster-level non-stationary correction for multiple comparisons (p < 0.05). The average local GMVs (left IFG/BA 45, right IFG) were then obtained using the “Extract ROIs signal” utilities implemented in REST [47]. To control for individual differences in whole brain size, the average relative GMVs obtained by dividing local GMVs by total gray matter volume was calculated. These average relative GMVs were then used as the dependent variables for all bivariate correlations (Figures 1B and 1D).

	Area	T score	MNI coordinate			Clusters size
			X	Y	Z
Positive correlation	Left IFG/BA 45	4.78	-50	31	15	266
	Right IFG	4.82	60	10	17	260
Negative correlation	No

Table 2. Regional GMV correlated with verbal creativity.

(voxels survived at clusters-level p<0.05，corrected with non-stationary)

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Figure 1. The relationship between regional GMV and verbal creativity.

(A) Statistical parametric mapping for the covariation between subjects’ verbal TTCT total score and regional GMV, the left IFG (BA45) is significantly positive associated with verbal TTCT total sore. The significant cluster is p < 0.05 nonstationary corrected with an underlying uncorrelated voxel level at p<0.0001. Structural maps shown at sagittal, coronal and axial sections are overlaid on the T1-weighted images. The significant cluster is shown at t > 3.8 for visualization purpose. (B) A scatterplot between verbal TTCT total score and relative GMV of the left IFG adjusted for age, gender, and general intelligence is shown for illustration purpose only. (C) The right IFG in which variability in regional GMV exhibited significant positive correlation with verbal TTCT total score is superimposed on a standard T1-weighted template brain in MNI stereotactic space. (D) A scatterplot between verbal TTCT total score and relative GMV of right IFG adjusted for age, gender, and general intelligence is shown for illustration purpose only.

https://doi.org/10.1371/journal.pone.0079272.g001

Correlation between WMVs and verbal creativity

Table 3 shows the correlation of WMVs with verbal TTCT. The regional WMVs of left IFG (x = -48, y = 34, z = 3; see also Figure 2A) and right IFG (x = 49, y = 6, z = 21; see also Figure 2C) were found to be significantly positively correlated with the total score of verbal TTCT. No negative correlation was found between regional WMV and the total score of verbal TTCT after multiple comparisons. All voxels survived at cluster-level non-stationary correction for multiple comparisons (p < 0.05). Figure 2 shows the bivariate correlations between relative WMVs in the left/right IFG and the verbal TTCT score. Relative WMVs were obtained using the same approach as that used for relative GMVs.

	Area	T score	MNI coordinate			Clusters size
			X	Y	Z
Positive correlation	Left IFG	4.50	-48	34	3	21
	Right IFG	4.43	49	6	21	44
Negative correlation	No

Table 3. Correlation between WMV and TTCT total score.

(voxels survived at clusters-level p<0.05 corrected with non-stationary)

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Figure 2. The relationship between regional WMV and verbal creativity.

(A) Statistical parametric mapping for the covariation between subjects’ verbal TTCT total score and regional WMV, the left IFG is significantly positive associated with verbal TTCT total sore. The significant cluster is p <0.05 nonstationary corrected with an underlying uncorrelated voxel level at p<0.0001. Structural maps shown at sagittal, coronal and axial sections are overlaid on the T1-weighted images. The significant cluster is shown at t > 3.8 for visualization purpose. (B) A scatterplot between verbal TTCT total score and relative WMV of the left IFG adjusted for age, gender, and general intelligence is shown for illustration purpose only. (C) The right IFG in which variability in regional WMV exhibited significant positive correlation with verbal TTCT total score is superimposed on a standard T1-weighted template brain in MNI stereotactic space. (D) A scatterplot between verbal TTCT total score and relative WMV of the right IFG adjusted for age, gender, and general intelligence is shown for illustration purpose only.

https://doi.org/10.1371/journal.pone.0079272.g002

Discussion

To address the association of cortical specialization to verbal creativity, the present study investigated the neural correlates of performance on verbal creativity tasks. The results of multiple linear regressions showed that increased regional GMV in the left IFG (BA45) and the right IFG is associated with verbal creativity measured by the verbal form of TTCT. Consistent with the assumption made in this study, the analysis demonstrated specificity to the prefrontal cortex. Existing evidences have also proven that prefrontal cortices are responsible for tasks requiring divergent thinking [9,20]. Furthermore, verbal creative performance was found to be positively correlated with regional WMVs in the left and right IFG as well.

With regard to gray matter structures, Takeuchi et al. (2010a) reported that individual differences in creativity (actually verbal creativity) were associated with regional GMV in the DLPFC and several cortical-subcortical regions. Fink et al. (2013) also reported that verbal creativity was significantly and positively associated with GMD in clusters within the right cuneus and the right precuneus. The lack of a relationship between verbal creativity and the prefrontal cortex is a slightly surprising finding in the work of Fink et al. (2013). The discrepancies in these results might be attributed to first, the methodological difference in the experiments. As the authors [Takeuchi et al. (2010a)] pointed out, the Standard VBM procedure applied in their experiment [in Fink et al. (2013) as well] had been criticized because of a few methodological limitations, such as the local misregistration of images in spatial normalization and a simple linear relationship assumed in segmentation [20]. This condition might result in several “pseudo-brain-correlates” that could not be replicated in a similar research. VBM with diffeomorphic anatomical registration was performed using exponentiated lie algebra (DARTEL) in our study. As described in the Method, DARTEL is proven as be an optimal VBM procedure that generates a more precise registration than the standard VBM procedure [38]. Meanwhile, a Bayesian framework was used to respectively carry out the probabilistic tissue classification (segmentation) and spatial non-linear deformation to Montreal Neurological Institute (MNI) space. In other words, the methodological limitations mentioned above were improved in our study. The brain correlates underlying verbal creativity—the subcortical regions in Takeuchi et al. (2010a) and the right cuneus and the right precuneus in Fink et al. (2013)—primarily might be the “pseudo-brain-correlates.” Second, the discrepancies in the results might be attributed to the different index measuring gray matter structures. We initially need to comprehend the different meanings of GMD and GMV. GMD represents the relative concentration of gray matter structures in spatially warped images (i.e., the proportion of gray matter relative to all tissue types within a region), whereas GMV represents the absolute amount of gray matter [48]. Several studies have indicated that the increase in GMV may be attributed to synaptogenesis, whereas the increase in WMV may be attributed to intracranial myelination [49,50]. Therefore, in regions where GMV increases but where GMD does not significantly change, the increase in GMV may be attributed to an increase in the number of synapses per neuron; a similar increase in the WMV due to myelination occurs simultaneously in these regions [48]. Both GMVs and WMVs in the bilateral prefrontal regions apparently increased with verbal creativity in the present study, whereas GMD in the regions did not significantly change with verbal creativity in Fink et al. (2013).

With regard to the white matter structures, the inconsistencies with previous studies were also observed. The paradoxical results of white structure related to creativity might be attributed to first, the difference in the experimental tasks. In Jung et al. (2010), both verbal and visuospatial divergent-thinking capacities were assessed, whereas in the present study and in Takeuchi et al. (2010b), only the verbal divergent-thinking capacity was assessed. Second, the paradoxical results might be attributed to the methodological difference in the experiments [FA derived from DTI in Jung et al. (2010) and Takeuchi et al. (2010b) vs. WMV derived from VBM in the present study]. A direct link between macroscopic neural structure (WMV) and microscopic neural structure (FA) in the human brain has yet to be established. What is known is that white matter structures are largely composed of nerve fibers called axons and fatty myelin sheaths around the axons [51]. As mentioned above, the increase in WMV may be attributed to intracranial myelination [46,47]. The myelination process allows neural signals to propagate more swiftly and with less signal loss. This aspect enhances connectivity within specific brain regions (the bilateral IFG here) and improves broader neural pathways connecting spatially separate regions required for many sensory, cognitive, and motor functions. The neural pathways are extremely complicated and require further research. Overall, the greater GMVs, together with the greater WMVs in the bilateral IFG, may reveal a greater neural computational efficiency in the regions.

The bilateral IFG (including BA 45) was the only region found to be associated with verbal creative thinking in the present study. To our knowledge, BA45, together with BA44, comprises Broca’s area, a region that is mainly involved in language production and comprehension, such as semantic generation tasks [52] and verbal fluency [53]. In one study, neuropsychological evidence revealed that patients with left prefrontal lesions exhibited impairment of the generation of verbal fluency [54]. Moreover, the role of the left inferior prefrontal cortex in ideas generation has been supported by a considerable amount of neuroimaging data [55,56]. In the present study, regional GMV in BA45 exhibited a positive correlation with verbal creativity. In other words, individuals with larger GMV in BA45 exhibited higher verbal creative than those with smaller GMV. Larger cortical volume is often linked to the improved computational efficacy of such region [57]. That is, the generation of verbal creative ideas may require a cerebral structural basis that can support effective semantic or concept generation. This view is consistent with the idea that creative processing requires cognitive control over conceptual knowledge networks as that are facilitated by the left ventrolateral prefrontal cortices [58]. In addition, the triangularis part of the left IFG has also been shown to play a role in the cognitive control of memory [59,60]. According to the “two-part” model of memory retrieval [60], we try to retrieve information in a top-down manner when we confront problems or tasks that must be solved. The retrieved knowledge is initially stored in the lateral temporal cortex, such as in the middle temporal gyrus. Recalling the top-down retrieval depends on conscious cognitive control. One can assume that a technique may be employed to exclude irrelevant data from the retrieval knowledge. To hone in on the desired information, some selection must occur. This selection is thought to occur post-retrieval in the left mid-ventral lateral prefrontal cortex (VLPFC), which corresponds to the location of the left IFG, specifically the pars triangularis [60]. Apparently, the process of excluding irrelevant information in top-down memory retrieval plays a crucial role in creative problems solving. The creative process entails activating remote conceptual networks selectively and inhibiting related semantic information [61]. For instance, a previous fMRI study suggested that the left IFG is recruited in the selection of more semantically distant demand [62]. The finding is in line with the idea that the generation of creative ideas involves remote conceptual association [23]. In another fMRI study (Fink et al., 2009), Alternative Use Task and name invention task asking for generating as original names as possible were applied. The two tasks were found to elicit consistently strong activation in the left IFG [9]. The authors suggested that the left IFG is responsible for the emergence of a new semantic representation in divergent thinking. Based on the findings of previous studies, the left IFG is believed to play a major role in the generation of semantic relatedness and in the selection of semantic relatedness. Generally, researchers believe in the existence of structural bases that underlies specific cognitive function. Hence, highly creative individual in the present study had larger GMV in the left IFG (i.e., pars triangularis).

The right IFG is commonly known to play a role in response inhibition [63-65]. Specifically, the right IFG is involved in inhibitory control over cognitive mental processing rather than in motor response control [65]. In addtion, strong evidence suggests that the right IFG also plays a role in attention switching [66,67]. As noted by Hampshire et al. (2010), the right IFG facilitated attention switching by inhibiting the previously attended object, location, or dimension. In this case, the attention shifts. To overcome the pre-potent response, a greater degree of inhibition is therefore necessary when switching attention away from a previous routine response, for example, during the generation of creative ideas. Flexible cognitive control, which is in the form of resistance from distraction (inhibitory control) and anttentional switch may be clearly necessary to sustain creative performance [68]. A recent patient study investigated the association between lesion locations and original responses using creative thinking tasks. Lesions in the right medial prefrontal cortex was found to be correlated with impaired originality [69]. This finding supports that of the current study, wherein highly creative individuals demonstrated larger GMV in the right IFG. In other words, the recruitment of cognitive control is beneficial to the creative process.

At last, the data of the present study did not reveal a dominant cerebral hemisphere in creative processing, as our present data shown. Dietrich and Kanso (2010) reviewed a total of 63 literatures and explored the neural underpinnings of creative behavior using either electroencephalographic techniques or neuroimaging techniques. Notably, these studies did not associated creativity with the right hemisphere or with any part of the right hemisphere, because creative processing does not rely on only a single, simple mental process or brain region. The present study supported this conclusion from a brain structural perspective. Regardless of the indicators of brain structure, i.e. GMVs or WMVs, both the left and right brain regions exhibited an obvious association with creativity.