Relations of Creativity to the Interplay Between High-order Cognitive Functions: Behavioral and Neural Evidence

Highlights

• Complex interplay between high-order cognitive functions underlies creativity.

• Creativity relates to the effect of cognitive control on episodic memory.

• Creativity relates to resting-state hippocampus-PFC functional connectivity.

• Anterior and posterior hippocampus are differentiated in supporting creativity.

Abstract

As a high-order cognitive ability, creativity is viewed as the result of complex interplay between a set of mental processes. However, previous studies have mainly tested one-to-one mutual relations between creativity and other cognitive abilities. It lacks studies to examine whether creativity is related to the interaction between cognitive systems. The current study aimed to fill this gap by testing the relations of creativity to the interactions between cognitive control and episodic memory systems using both behavioral and neuroimaging methods. The Alternative Uses Task was used to measure the divergent component of creativity. A computer-based behavioral task was used to measure cognitive control, episodic memory, and their interactions. Additionally, the interactions between cognitive systems were characterized by computing the resting-state functional connectivity between hippocampus and prefrontal regions, which are the neural substrates for episodic memory and cognitive control, respectively. By analyzing these behavioral and neuroimaging data, the behavioral results indicated that creativity was significantly related to the effect of cognitive control induced by switching tasks or proactive cues on subsequent memories of items or sources. Additionally, neuroimaging results showed that creativity was significantly related to the connectivity from hippocampus to both left superior frontal gyrus and middle frontal gyrus. Such relations were also differentiated between anterior and posterior hippocampus. Altogether, these findings suggest that creativity is related to interactions between cognitive control and episodic memory, supporting the claim that creativity is the result of complex interplay between high-order cognitive functions.

Introduction

Creativity is commonly defined as “the ability to produce work that is both novel (i.e., original, unexpected) and appropriate (i.e., useful, adaptive concerning task constraints)” (Sternberg and Lubart, 1999, p. 3). A large number of studies on creativity have focused on the divergent component, which refers to the generation of diverse, novel, or unique ideas or solutions for an open-ended problem. For example, in the Alternative Uses Task (AUT), open-ended questions are provided and individuals are encouraged to generate multiple answers, the novelty and appropriateness of which are used to rate creativity (Guilford, 1967).

Recently, there is a surge of interest in the cognitive processes involved in creativity (Beaty et al., 2019, Benedek and Fink, 2019). Theoretically, it is widely accepted that creativity doesn’t rely on a single cognitive system, but the interplay between a set of mental processes (Beaty et al., 2016, Beaty and Schacter, 2018). However, as previous studies have mainly focused on investigating one-to-one mutual relations between creativity and other cognitive abilities, there is still a lack of studies to provide behavioral and neural evidence for the relations of creativity to the interactions between cognitive systems. To provide insight into this question, this study examined the relations of creativity to the interplay between cognitive control and episodic memory.

In some early studies, creativity was viewed as a mysterious and uncontrollable mental activity that mainly relies on sudden inspiration, spontaneous, and undirected thoughts (Gardner, 1982, Kasof and Joseph, 1997, Amer et al., 2016). Recently, a lot of behavioral and neurological evidence has suggested the dynamic regulation role of cognitive control on creativity (Radel et al., 2015, Chrysikou, 2018). Top-down cognitive control has been found to participate in the generation of creative ideas. During this process, cognitive control may direct top-down attention to retrieve information in goal-directed way, select effective strategies flexibly, and inhibit the salient but unoriginal ideas that may be driven by bottom-up attention (Hommel et al., 2011, Benedek et al., 2012, Chrysikou, 2018, Benedek and Fink, 2019).

Relations of creativity to cognitive control and related cognitive abilities have been supported by behavioral evidence (e.g., Chrysikou, 2019, Zabelina and Robinson, 2010). For example, individuals who performed better in creative thinking test scored higher on the indexes of cognitive control (Groborz and Necka, 2003). Moreover, creativity was also found to be related to the subcomponents of cognitive control, including inhibition, updating, and working memory (Benedek et al., 2014a, Benedek et al., 2014b, Chrysikou, 2019). For instance, working memory capacity was positively related to creative performance on divergent thinking tasks that required participants to generate a word associated with all three given items (Nijstad et al., 2010, de Dreu et al., 2012). Additionally, inhibition was positively related to the originality of generated ideas or drawings, and both updating and inhibition components predicted AUT task performance (Benedek et al., 2014a, Benedek et al., 2014b, Edl et al., 2014). Altogether, these findings suggest that highly creative individuals are possibly more effective at suppressing irrelevant responses as well as maintaining and updating related information than individuals with low creativity.

The relations between creativity and cognitive control have also received support from neuroimaging findings. Prefrontal cortex (PFC) is one of the brain regions supporting cognitive control functions (Miller, 2000, Koechlin et al., 2003, Chrysikou, 2018). Meantime, PFC has been reliably found to participate in the process of creative thinking (Dietrich, 2004, Dietrich and Kanso, 2010, Kleibeuker et al., 2013). For example, after reviewing 45 brain-imaging studies, researchers found that PFC showed significant and consistent activation across different divergent thinking tasks (Arden et al., 2010). Additionally, EEG results also showed that generating creative ideas increased frontal alpha synchronization that reflects the active inhibition of task-irrelevant distractors (Sauseng et al., 2005, Fink and Benedek, 2014). Another ERP study found that divergent thinking was associated with higher attentional flexibility, which generally relies upon cognitive control to switch between different attentional status (Zabelina and Ganis, 2018). Furthermore, a meta-analysis of 34 functional MRI studies distinguished the contribution of PFC subregions to performing various creative tasks (Gonen-Yaacovi et al., 2013). Specifically, the caudal dorsolateral PFC was related to the generation of creative ideas, whereas the lateral rostral PFC was related to the flexible combination of information, suggesting that different PFC subregions have functional specificity in supporting creativity (Gonen-Yaacovi et al., 2013).

Creative thinking involves the process of forming associative concepts into new combinations during the idea generation process, suggesting the retrieval and reorganization of concepts stored in long-term semantic memory (Mednick, 1962). Recently, the focus of studies on creativity has shifted from semantic memory to episodic memory, a neurocognitive system that supports the memories of events and related contextual details (Shi et al., 2020). In general, both remembering past experiences and imagining future experiences rely heavily on episodic memory (Schacter and Madore, 2016). The involvement of episodic memory in creative cognition has received support from behavioral and neural findings (Abraham, 2013, Beaty and Schacter, 2018).

A behavioral study found that during the generation of unusual uses for common objects in the AUT task, some initial responses were derived by retrieving episodic memory (Gilhooly et al., 2007). Additionally, before performing the AUT task, a brief training in recollecting details of a recent event had positive impact on subsequent creative performance (Madore et al., 2015), suggesting that training episodic memory enhanced the generation of creative ideas. Moreover, the AUT performance was positively associated with the amount of episodic details generated from the imagination of future events (Addis et al., 2016).

Hippocampus, as a critical region supporting episodic memory (Mullally and Maguire, 2014, Canada et al., 2019), was found to be involved in creative cognition. For example, hippocampus showed increased activation in the AUT task (Benedek et al., 2014a, Benedek et al., 2014b). Clinical study demonstrated that hippocampal amnesic patients performed poorly on divergent thinking tasks, such as creating novel drawings, generating unusual uses for specific item (Duff et al., 2013), or listing associated words for cue words varied in open-endedness (Sheldon et al., 2013), suggesting that the cognitive functions supported by hippocampus were indispensable for creativity. Additionally, a recent study found that inhibiting hippocampal activity through fMRI-guided transcranial magnetic stimulation reduced creative ideas and episodic details (Thakral et al., 2020).

Benedek and Fink (2019) proposed a neurocognitive framework claiming that creative cognition is the result of the interplay between memory, attention, and cognitive control. This claim has received much support, especially in terms of the interaction between cognitive control and episodic memory. First, it was found that cognitive control, reactively induced by task switching, impaired the memory of task-related information but benefited the memory of task-unrelated information (Richter and Yeung, 2012). Furthermore, the authors found that cognitive control recruited proactively (i.e., proactive control) was beneficial to the encoding of relevant information but impaired the processing of irrelevant information (Richter and Yeung, 2015). Neurologically, PFC, as a brain region highly related to cognitive control, has been reliably found to participate in the encoding and retrieval processes of episodic memory (Fletcher et al., 1998, Nolde et al., 1998, Wagner, 2002, Eichenbaum, 2017). Therefore, past studies have provided strong evidence to support the close relations between cognitive control and episodic memory.

Additionally, the connections between brain regions or networks that are highly related to cognitive control or episodic memory have been found to be related to creativity (Schnotz and Bannert, 2003, Jung et al., 2013). For example, during the generation and evaluation of creative ideas, there were intense interactions between default mode network (DMN, involving brain regions critical for episodic memory, such as hippocampus) and cognitive control network (Beaty et al., 2016, Beaty and Schacter, 2018). The functional connectivity between these brain networks can reliably predict individual creative thinking (Beaty et al., 2019). Both DMN and cognitive control network were found to be the core hubs of the distributed network activated during performing the divergent thinking task. Especially, in the later stage of the task, there was an increased coupling between the brain regions within these networks (Beaty et al., 2015). Such finding has also been replicated in special populations with creative talent. For example, visual artists showed greater positive functional connectivity between cognitive control network and DMN during the evaluation process versus the generation process of making creative products (Ellamil et al., 2012). Moreover, when more creative people performed divergent thinking tasks, the coupling activation between DMN and ventral anterior cingulate cortex, a region related to cognitive control, was enhanced compared to less creative people (Mayseless et al., 2015).

Despite a large number of behavioral and neuroimaging studies on creativity and its relations with other cognitive abilities, it still lacks of studies to directly test the relation of creativity to the interplay between cognitive control and episodic memory. Specifically, it is unknown whether creativity is related to the effect of cognitive control on episodic memory. Neurologically, hippocampus, as a critical brain structure in DMN, is essential for both episodic memory and creative thinking (Cabeza et al., 2020). Studies have consistently found that hippocampus can be functionally differentiated into anterior and posterior regions and each subregion is responsible for specific cognitive functions (Moser and Moser, 1998). For instance, it has been proposed that while anterior hippocampus processes global information in a coarse way, the posterior hippocampus usually processes local information in a fine-grained way (Evensmoen et al., 2013, Nadel et al., 2013). Such functional heterogeneity of hippocampal subregions is also involved in creative cognition. For example, a study found that after performing the AUT task, the functional connectivity between anterior hippocampus and frontal regions (i.e., ventrolateral prefrontal cortex, VLPC) became stronger (Madore et al., 2019), suggesting that anterior and posterior hippocampus may play different roles in supporting creativity. However, the relation of creativity to the differences between anterior and posterior hippocampus in their connectivity to other brain regions has not been empirically examined.

The purpose of this study was to explore the relations of creativity to the interplay between 2 high-order cognitive functions: episodic memory and cognitive control. First, we examined the relation of creativity to the effect of cognitive control on episodic memory by using computer-based behavioral task. Then, we tested whether creativity was related to the resting-state functional connectivity between hippocampus and other brain regions related to cognitive control. Finally, we examined whether creativity was related to the functional differentiation between anterior and posterior hippocampus. We predicted that creativity would be related to the effect of cognitive control on episodic memory, the resting-state functional connectivity between hippocampus and PFC regions, and hippocampal functional differentiation.