Cerebral blood flow associated with creative performance: A comparative study

Abstract

Creativity is important for social survival and individual wellbeing; science, art, philosophy and technology have been enriched and expanded by this trait. To our knowledge this is the first study probing differences in brain cerebral blood flow (CBF) between highly creative individuals (scientists and/or artists socially recognized for their contributions to their fields with creativity indexes corresponding to the 99% percentile) and average control subjects while performing a verbal task from the Torrance Tests of Creative Thinking. Additionally, we correlated CBF with creativity dimensions such as fluency, originality and flexibility. Subjects with a high creative performance showed greater CBF activity in right precentral gyrus, right culmen, left and right middle frontal gyrus, right frontal rectal gyrus, left frontal orbital gyrus, and left inferior gyrus (BA 6, 10, 11, 47, 20), and cerebellum; confirming bilateral cerebral contribution. These structures have been involved in cognition, emotion, working memory, and novelty response. The score on the three creativity dimensions – fluency, originality, and flexibility– correlated with CBF activation in right middle frontal gyrus and right rectal gyrus (Brodmann Area 6, 11). Moreover, fluency and flexibility strongly correlated with CBF in left inferior frontal gyrus and originality correlated with CBF in left superior temporal gyrus and cerebellar tonsil. These findings suggest an integration of perceptual, volitional, cognitive and emotional processes in creativity. The higher CBF found in particular brain regions of highly creative individuals during the performance of a creative task provides evidence of a specific neural network related to the creative process.

Introduction

Creativity plays a crucial role in cultural life and also in individual development and well being. It involves pleasure, which enables individuals to persevere in their creations over time in spite of difficulties or rejection. Understanding how creativity occurs and which brain processes are involved with it is a challenging task, and such an understanding might transform our view of ourselves and our societies (Zeki, 2001). In the 19th century, creativity was first considered as a biological trait (Galton, 1892). Also at that time it was proposed that there was a high rate of synaesthesia (when a sense is experienced in the modality of another sense; for example, tasting shape, or hearing color) among highly creative individuals (Galton, 1880). Furthermore, it was suggested that geniality is related with an altered neurophysiology. However, it was not until the beginning of the 21st century that scientists realized that complete theories of creativity and aesthetics should be neurobiologically based and a new research field called neuroesthetics was established (Zeki, 2001).

Creativity means bringing into being; it involves generation of novelty and transformation of the existent. There have been proposed theoretical models describing stages or dimensions of the creative process. That is the case of the association integration–elaboration–communication phenomenological model (Chávez, 1999, Chávez, 2004). This model was developed from phenomenological observations of poets and deep phenomenological interview with scientists, writers, music composers, and plastic artists. The first stage of this model involves the association of previously unrelated elements of inner and outer experiences. Sensorial, cognitive, and affective integrations take place involving different degrees of consciousness. This phase includes (a) episodes of automatic creation (what has been called inspiration), (b) sudden insight (also known as illumination) achieved when we perform any other apparently unrelated activity, a process that has been named incubation (Wallas, 1926, Boden, 1994, Torrance and Safter, 1999), and (c) conscious combination of elements. The phase of elaboration involves the following conscious work invested in the ideas gained through the previous phase and involves volition. The phase of communication allows transmitting the associations, often unleashing new creative processes in other individuals, making creativity “contagious.” Margaret Boden (1994), an influential author in the field differentiated between two types of creativity: psychological creativity P and historic creativity H. P creativity occurs in one person’s mind and it does not matter if other people already had that idea; H creativity is new for the person but also for humanity. Several external factors (such as fashion, rivals, disease, economy, and war, among others) influence the survival overtime of this kind of creativity; for that reason, there cannot be a single and systematic explanation for H creativity, but all H creativity is P creativity by definition; therefore, an explanation of P creativity will include H creativity as well (Boden, 1994).

Considering the complexity of creativity, some researchers have focused on specific characteristics of creative products whereas others consider specific parts of the creative process in order to assess creativity. Regarding the latter, the Torrance Tests of Creative Thinking (TTCT) are standardized psychometric tests evaluating creative performance (Torrance, 1990); the TTCT provide standard stimuli from which the creative process is reproduced in controlled environments. The TTCT are based on the evaluation of divergent thinking (Guilford, 1968), the production of a variety of responses not determined by explicitly given information. A normal distribution of the creativity index in the general population has been reported using these tests, finding no significant differences between genders (Torrance, 1990, Torrance and Safter, 1999). Specific forms of cognition have been identified in highly creative individuals. These are: (1) divergent thinking, proposed by the cognitive psychologist J. P. Guilford (1968). Divergent thinking is a style of thinking that produces a number of different possible answers, opposed to convergent thinking, which leads to a single correct answer (what most intelligence tests evaluate). Even if divergent thinking is a necessary condition for creative achievement, convergent thinking is also required in order to facilitate appropriate responses and suppress inappropriate ones, particularly during the elaboration phase of the creative process (Guilford, 1968). (2) The bisociation of no-related matrixes, proposed by the writer Arthur Koestler. The bisociation of no-related matrixes is the ability to connect previously unrelated skills or matrixes of thought (Koestler, 1964). (3) The janusian and homospatial processes, identified by the psychiatrist Albert Rothenberg after evaluating dozens of individuals awarded with the Nobel Prize. The homospatial process involves superimposition of discrete entities, which may be visual or other kinds of mental representations. The janusian process consists of actively conceiving multiple opposites or antitheses simultaneously (Rothenberg, 2000). (4) The tertiary process, proposed by the psychoanalyst Silvano Arieti, is the integration of primary and secondary processes simultaneously (Arieti, 1976). Secondary process refers to logical thinking. Primary process is present in dreams and in psychotic thinking, but also in works of art; scientists such as Einstein, Loewi, Kekulé, and Mendeleyev seem to have used it during some phases of their creative production (Root-Bernstein and Root-Bernstein, 1999, Mazzarello, 2000). Primary process cognition has been related to right cerebral hemisphere activation whereas secondary process has been related to left hemisphere activation (Martindale et al., 1984). Highly creative individuals have a tendency to be physiologically overreactive to stimulation. For instance, when compared to less creative subjects the highly creative exhibit prolonged alpha electroencephalographic (EEG) blocking in response to tones; they habituate slower to stimuli; and they rate electric shocks as being more painful (Martindale, 1978, Martindale et al., 1984, Martindale et al., 1996). In addition, large and consistent EEG differences between high and low creative individuals have been observed only during creative task performance. Less creative subjects tend to show alpha blocking on all types of cognitive tasks, including creative tasks, while highly creative individuals tend to be differentially reactive. During non-creative tasks highly creative individuals also exhibit alpha blocking. However, they tend to operate at a relatively low level of arousal and to show alpha enhancement during creative tasks (Martindale, 1978). The right-hemisphere EEG activity in parieto-temporal areas tends to be significantly higher than left-hemisphere activity in highly creative individuals specifically during creative tasks performance (Martindale et al., 1984, Martindale, 1990). Nonetheless, it was found that more creative individuals exhibited higher alpha indices during an analog of creative inspiration (the association phase) than during an analog of creative elaboration. This pattern was not found in less creative subjects (Martindale and Hasenfus, 1978).

When comparing regional cerebral blood flow (rCBF) between low and highly creative individuals during the performance of creative tasks, highly creative subjects tend to show more bilateral prefrontal rCBF whereas low creative individuals display functions predominantly in the left cerebral hemisphere (Carlsson et al., 2000). Another study compared the results of EEG and CBF measures from two different populations. These individuals were administered the same verbal creative tasks. It was found that greater creative performance was related to higher values of spatial synchronization in anterior cortical areas and a general increase of the coherence in both frontal areas. Highly creative performance was also associated with higher CBF in both frontal lobes, particularly Brodmann Areas (BA) 8–11 and 44–47 (Bekhtereva et al., 2001). In contrast to Carlsson et al. (2000) research, in this study individuals were not selected using creativity index scores. In a later CBF PET study (Bekhtereva et al., 2004) the authors evaluated 25 healthy subjects recruited from the general population administering two different cognitive strategies of creativity: the first strategy consisted in composing a story using a list of words from different semantic areas; the second strategy involved filling gaps between words and making logical associations. Creative performance correlated with activation in the left parieto-temporal regions (BA 39 and 40).

A previous study conducted by our research team found positive significant correlation between the figural and verbal creativity indexes and the cerebral blood flow in the right anterior cerebellum and the right precentral gyrus (BA 6), the right postcentral gyrus (BA 3), the left middle frontal gyrus (BA 11), the right rectal gyrus (BA 11), the right inferior parietal lobule (BA 40), and the right parahippocampal gyrus (BA 35). These brain areas are involved in multimodal processing, in complex cognitive functions such as imagery, association processes, memory and novelty processing, among others (Chávez et al., 2004).

Jung-Beeman et al. (2004) conducted an fMRI study using a modified form of Mednick’s test of creative cognition where subjects encountered three problem words and attempted to produce a single solution word. They found that solving problems with a subjective feeling of insight activated a complex cortical network; the right anterior superior temporal gyrus was a key component. Using EEG they found a sudden burst of high frequency (gamma band) neural activity in right anterior superior temporal area prior to insight solutions. The right anterior temporal gyrus has been associated with making connections across distantly related information (Jung-Beeman et al., 2004).

Vartanian and Goel, 2005, Vartanian and Goel, 2007 conducted fMRI studies seeking to determine if the right and left prefrontal cortex (PFC) would engage differently when generating hypothesis, a key feature of creative cognition. For this purpose they used a modification of Guilford’s classic match problems; a good performance involves the ability of making set shifts or movements from one state in a problem space to a horizontally displaced state, referred as lateral transformations by these researchers. The generation of hypothesis that required set shifts activated the right ventral lateral PFC (BA 47), left middle frontal gyrus (BA 9), and left frontal pole (BA 10). The activation in right dorsal lateral PFC (BA 46) and cerebellum covariated as a function of the number of solutions that were generated (Goel and Vartanian, 2005). A later study using anagram problems confirmed the involvement of right ventral lateral PFC (BA 47) with hypothesis generation (Vartanian and Goel, 2005, Vartanian and Goel, 2007).

Gómez-Beldarrain et al. evaluated 18 patients with PFC lesions finding an impairment of counterfactual thinking (mental simulations of what might have been if another behavior had been executed). Counterfactual thinking correlated positively with creativity measures (design fluency test). The researchers conclude that the PFC is crucial only for the spontaneous generation of counterfactual thinking (Gomez-Beldarrain et al., 2005).

Howard-Jones et al. (2005) performed an fMRI investigation (Howard-Jones et al., 2005) in 8 healthy undergraduate and graduate students and required them to produce creative and uncreative stories from related and unrelated word sets finding that when participants were being creative there was an increase in activity in the prefrontal areas, in particular right medial frontal gyrus (BA 9 and 10); additional activity in these areas was observed when using unrelated word sets. The authors suggest that these prefrontal areas are involved with the divergent semantic processing associated with creativity.

The aims of the present research were to compare the CBF between average and highly creative individuals during the performance of a creative task and to correlate the CBF with the scores on creativity dimensions (fluency, originality, and flexibility) using Single Photon Emission Computerized Tomography (SPECT) and statistical parametric mapping. Our a priori areas were the fronto-temporal regions because of their involvement in cognitive and emotional functions that are critical to the creative process.