Brain hemispheric involvement in visuospatial and verbal divergent thinking

Highlights

• Individuals with increased segregation in the right visual and sensorimotor networks show higher VSDT.

• Individuals with reduced lateralization within frontal and temporoparietal regions show higher VDT.

• Two distinct forms of functional lateralization in visuospatial and verbal divergent thinking.

Abstract

Hemispheric lateralization for creative thinking remains a controversial topic. Early behavioral and neuroimaging research supported right hemisphere dominance in creative thinking, but more recent evidence suggests the left hemisphere plays an equally important role. In addition, the extent to which hemispheric lateralization in specific brain regions relates to individual creative ability, and whether hemispheric dominance relates to distinct task performance, remain poorly understood. Here, using multivariate predictive modeling of resting-state functional MRI data in a large sample of adults (N = 502), we estimated hemispheric segregation and integration for each brain region and investigated these lateralization indices with respect to individual differences in visuospatial and verbal divergent thinking. Our analyses revealed that individual visuospatial divergent thinking performance could be predicted by right-hemispheric segregation within the visual network, sensorimotor network, and some regions within the default mode network. High visuospatial divergent thinking was related to stronger functional connectivity between the visual network, fronto-parietal network, and default mode network within the right hemisphere. In contrast, high verbal divergent thinking performance could be predicted by inter-hemispheric balance within regions mainly involved in complex semantic processing (e.g., lateral temporal cortex and inferior frontal gyrus) and cognitive control processing (e.g., inferior frontal gyrus, middle frontal cortex, and superior parietal lobule). The current study suggests that two distinct forms of functional lateralization support individual differences in visuospatial and verbal divergent thinking. These findings have important implications for our understanding of hemispheric interaction mechanisms of creative thinking.

Introduction

Hemispheric lateralization or asymmetry is considered to result from an evolutionary conservation mechanism allowing fast and efficient information processing in the human brain (Duboc et al., 2015; Levy, 1969; Toga and Thompson, 2003; Wang et al., 2014). Several studies have demonstrated subtle structural or functional differences between the two hemispheres corresponding to dominant processing of specific cognitive tasks (Duboc et al., 2015). One of the cognitive processes hypothesized to show hemispheric dominance is creative thought (McCallum and Glynn, 1979) which is generally defined as an ability to come up with novel and useful ideas to open-ended problems (Runco and Jaeger, 2012; Sternberg and Lubart, 1996). A long-standing yet controversial theory suggests that creativity results solely from right hemisphere processes (Bowden and Beeman, 1998; Bowden and Jung-Beeman, 2003; Torrance, 1982; Wheatley, 1977), while a moderate view emphasizes a right-hemisphere advantage in figurative or metaphoric thinking (i.e., coarse semantic coding), presumably facilitating novel and original idea production (Beeman et al., 2000; Folley and Park, 2005; Zhao et al., 2014). An alternate view suggests that creative thinking involves the interaction and integration of information from both hemispheres (Atchley et al., 1999; Carlsson et al., 2000; Lindell, 2011). Although the relationship between creative thinking and hemispheric differences is often emphasized in the literature (Lindell, 2011; Mihov et al., 2010; Moore et al., 2009), patterns of hemispheric lateralization support creativity in different modalities (e.g., verbal and figural) remains an open question.

Visual creativity requires people to output the production (e.g., via drawing) of novel and useful visual forms, a process thought to involve divergent thinking (Aziz-Zadeh et al., 2012; Dake, 1991). Previous neuroimaging studies have found that the right hemisphere was more strongly engaged during visuospatial (i.e., figural) creative thinking (Bhattacharya and Petsche, 2002; Gansler et al., 2011; Kenett et al., 2015; Kowatari et al., 2009; Miller et al., 2000; Miller and Hou, 2004). A common view proposes that the right hemisphere may attenuate inhibitory process from the left hemisphere (Mayseless et al., 2014). Furthermore, lesion studies have linked left-lateralized brain disorders or lesions, such as frontotemporal lobe dementia (FTD), to a “release” of right frontal and posterior cognitive functions previously shown to enhance creative drawing (Miller and Hou, 2004; Seeley et al., 2007). However, recent studies have shown higher activation within left fronto-parietal brain regions, premotor cortex, inferior frontal cortex, and lateral occipital gyrus associated with visuospatial creativity (Aziz-Zadeh et al., 2012; Huang et al., 2013; Saggar et al., 2015). While a clear consensus has not emerged from such studies, the existing research more generally has shown that the right hemisphere may play a critical role in visual creativity. Thus, the asymmetries of the right hemisphere compared with left may facilitate visuospatial (i.e., figural) creative thinking.

Similarly, verbal creativity refers to the ability to generate novel and useful solutions through verbal forms such as oral response or writing down ideas. According to the coarse semantic coding hypothesis, the right hemisphere is more specialized for processing loosely-related semantic information than the left hemisphere (Beeman and Bowden, 2000; Kounios and Beeman, 2014). However, recent views hold that verbal creativity benefits from the interaction and integration of information from both hemispheres (Lindell, 2011; Takeuchi et al., 2010). Past work has shown that the two cerebral hemispheres code semantic information in different ways (Jung et al., 2013; Mirous and Beeman, 2012). Bilateral temporo-parietal regions are thought to be crucial for semantic activation, whereas the right anterior middle/superior temporal gyrus and inferior frontal gyrus may contribute to semantic integration and selection, respectively (Jung-Beeman, 2005). Accordingly, verbal creativity may be based on the interaction or integration between both hemispheres, rather than only depend on the right hemisphere. More recently, Faust and Kenett (2014) postulated that semantic processing involves the whole brain and thus creative verbal processing requires efficient semantic integration that is achieved via well-balanced hemispheric communication (Faust and Kenett, 2014).

In the present research, we employed resting-state fMRI to assess whether high-creative thinking ability results from neuropsychological markers of cerebral lateralization. Particularly, recent neuroimaging studies using resting-state fMRI data indicated that left-hemisphere regions are biased to interact more strongly within the same hemisphere—such as the fronto-parietal control network preferentially coupling to the default network and language-related regions in the left hemisphere—whereas right-hemisphere regions interact more strongly with both hemispheres (Gotts et al., 2013; Wang et al., 2014). Importantly, the magnitude of lateralization measured for individual participants in these regions predicted the level of cognitive ability, such as language and motor abilities (associated with a left-lateralization; Amunts et al., 1996; Joliot et al., 2016) and visuospatial attention (associated with right-lateralized; Cai et al., 2013; Wang et al., 2016). In the light of these findings, we hypothesized that if functional lateralization benefits creative thinking ability—as has been suggested in theories and popular culture of creative individuals as being “right-brained”—a quantitative relationship should exist between the strength of lateralization and the level of creative thinking. We tested two hypotheses regarding the relationship between hemispheric lateralization and creative thinking. First, hemispheric segregation benefits creative thinking, which is consistent with previous research reporting reduced inter-hemispheric connectivity between brain areas and increased right-hemispheric connectivity during rest in highly-creative individuals (Lotze et al., 2014). Second, well-balanced inter-hemispheric processing benefits creative thinking, supported by evidence that creativity does not appear to depend on activation differences between hemispheres (Badzakova-Trajkov et al., 2011), but rather balanced hemispheric activation (Mayseless and Shamay-Tsoory, 2015; Shamay-Tsoory et al., 2011).

Furthermore, the current study explored the relationship between hemisphere lateralization and domain performance of creative thinking. According to previous findings, we hypothesized that individuals with high segregation of right frontal-parietal and visual networks displayed enhanced visuospatial creative performance, whereas individuals with high inter-hemispheric integration of frontal-temporal and fronto-parietal networks will show higher verbal creative performance. Together, the present study provides the novel evidence of the extent to which verbal and visuospatial creative ability involve different hemispheres of the brain.