Abstract

Creativity is the new discovery, understanding, development and expression of orderly and meaningful relationships. Creativity has three major stages: preparation, the development (nature and nurture) of critical knowledge and skills; innovation, the development of a creative solution; and creative production. Successful preparation requires a basic level of general intelligence and domain specific knowledge and skills and highly creative people may have anatomic alterations of specific neocortical regions. Innovation requires disengagement and divergent thinking primarily mediated by frontal networks. Creative people are often risk-takers and novelty seekers, behaviors that activate their ventral striatal reward system. Innovation also requires associative and convergent thinking, activities that are dependent on the integration of highly distributed networks. People are often most creative when they are in mental states associated with reduced levels of brain norepinephrine, which may enhance the communication between distributed networks. We, however, need to learn more about the brain mechanisms of creativity.

Introduction

Creative innovations have enriched peoples' lives, prolonged peoples' life, and have helped to relieve suffering. For example, when I was an infant in 1939, I developed a fever, and a stiff neck. My pediatrician diagnosed meningococcal meningitis which was a fatal disease. My pediatrician had a faculty appointment at one of the medical schools in New York City where they were doing research trials with new medications called sulfanilamides, also called sulfa drugs. He was able to get this medication and treat me. This same medication also helped to save the life of the son of President Franklin Delano Roosevelt, as well as many other people who had terrible infections. If I had been born a few years earlier, or sulfa drugs were not invented, I would not be writing this article.

One of the major reasons that some nations and cultures have been more successful than others is often related to their creativity. Unfortunately, part of this success has been related to the creation of instruments of war, but creativity also has important economic implications. For example, as Richard Florida notes in his influential book “The Rise of the Creative Class” (2002), countries such as the United States cannot compete with other less affluent countries for an inexpensive labor market. Our economy has been and will be increasingly dependent upon creativity, and it is those who are creative that are often the people who are most likely to be successful.

In 1960, Jane Goodall reported that she observed a chimp that broke off a branch of a tree and took leaves off this branch in order to make a tool which this chimp could insert into a termite mound to obtain the termites which chimps enjoy eating. Although this chip performed a creative act, for the most part the only animal who exhibits creativity is the human. Much research has been performed on the brain mechanisms that mediate human cognitive abilities such as language, but there is still little known about the brain mechanisms of creativity. Nonetheless, this article will attempt to provide a brief overview of what is known about the human brain mechanisms mediating creativity.

Definition

Although dictionaries often define creativity by using terms such as “productive, original, and of value,” this definition is incomplete. Great creative works have another important element perhaps best described by Bronowski (1972) who defined creativity as “the ability to find unity in what appears to be diversity” or stated in another way, “finding the thread that unites.” The great creative works of art, in addition to being novel, often have a myriad of colors, shapes, and textures, but in these great paintings, all this diversity comes together. Moreover, great paintings have a unity with closure. Great musical scores have many different auditory tones, with different durations and amplitude, but again there is a thread that units them. This also holds true for great pieces of literature. Great scientists, who made paradigmatic shifts such as Einstein, Copernicus, and Newton, developed theories that found the thread that unites. For example, Einstein described the thread that unites matter and energy. By positing a heliocentric system, Copernicus was able to explain the motion of the planets. However, as will be discussed in this review, creativity requires more that “finding unity.” Thus, I have suggested that creativity be defined as the new discovery or understanding, development, and expression of orderly relationships (Heilman, 2005).

Stages of Creativity

Because creativity is a cognitive process and these processes often take place in organized stages, Helmholtz (1826) and Wallas (1926) suggested that creativity has four stages. The first stage is “preparation,” and in this stage, a person develops the knowledge and skills needed to discover, develop, and produce a creative product. This development depends on two major factors exposure–experience–learning and the brain's ability to store, process, and use this knowledge. The next stage is what they termed “incubation.” This is the stage where a person's brain nonconsciously searches for an answer or attempts to find unity. The third stage is called “illumination.” This is the state where a person discovers the answer and finds unity. Illumination is sometimes called the “ah-ha” experience, and when Archimedes discovered the law of buoyancy in the bathtub he yelled “Eureka!” The final step in the creative process is the production of the work of art, literature or music or in science, tests of new theories, and publication of the results. This last stage is one of “production and/or verification.”

Many great discoveries were not made by using the nonconscious mind, but rather by a series of conscious steps. In addition, sometimes the prepared mind sees an anomaly and observing this anomaly helps to produce an illumination. For example, the discovery of penicillin was based on Fleming's observation of a mold that flew through his open window, landed on bacterial culture, and killed the bacteria. Because many great creative ideas take place with conscious steps, as well as the observations of anomalies, not all great creative discoveries require incubation. Thus in our prior reports (Heilman, 2005; Heilman, Nadeau, & Beversdorf, 2003), we have combined the incubation and illumination stages into one stage which we call the “innovative” stage.

This review will focus on the first two states of creativity: preparation and innovation.

Preparation

Intelligence

If a person is going to be creative, he/she need to acquire knowledge and skills. The acquisition of this knowledge and skills depends on two major factors, nature and nurture. Some have called the ability to acquire and use knowledge intelligence, and intelligence is often considered a critical element of creativity. Historically, several of the people who develop intelligence tests were attempting to develop a test that could predict a child's ability to be creative. Lewis Terman chose term “genius” as the classification label for the people with high scores on intelligence tests (135 or higher) such as the Stanford-Binet intelligence test which he helped to devise (Terman, 1916). Terman and Oden (1959) collected a group of children from northern California who scored very high on this IQ test and thus were identified as “geniuses.” These highly intelligent children were followed as they matured to adults and whereas most of these people turned out to be very successful, Terman's group of geniuses did not have many people who were noted to be extremely creative. One of the children who had their intelligence tested, but not included in Terman's group because his IQ was lower than the criteria set by Terman, was William Shockley who went on to win the Nobel prize in physics because of his invention of the transistor. Another person tested who received a Nobel Prize in physics, but was not included in Terman's group of geniuses because his IQ was too low, was Luis Walter Alvarez who helped to develop radar during the Second World War, worked on the Manhattan Project, and designed the liquid hydrogen bubble chamber that helps to measure particle interactions. There are many other examples of people such as Richard Feynman, who won a Nobel Prize in physics and became widely known as a genius; however, Feynman's IQ was 125, which is below Terman's criteria for being a “genius.”

The term “genius” comes from Latin and means “to beget, bring forth” or to create, and this Stanford-Binet intelligence test does not assess creativity. Subsequent studies also found only a weak relationship between creativity and IQ (Barron and Harrington, 1981) and that depending on the domain of creativity, there may be IQ thresholds, but after that IQ threshold is reached, the person's IQ does not predict creativity. Most IQ tests assess what has been learned and retrieved from stored knowledge by requiring the test taker to find the correct answers (word definitions) or to use convergent reasoning (similarities). However, as will be discussed, creativity is very dependent on processes such as disengagement and divergent thinking. For example, intelligence would be knowing that a brick is used to construct buildings, but divergent reasoning might allow a person to use a brick to play shuffleboard or used to remove callouses from the feet after a bath.

Special Talents and Skills

The postulate that the human brain was organized in modular fashion was first put forth by Franz Gall in the early part of the 19th century (Gall & Spurzheim, 1810–1819). Gall also reasoned that if certain brain functions are mediated by specific anatomic areas, then the more brain tissue a person has devoted to this function, the better this person would perform this function. The size of the brain region influences the shape of the skull overlying this area, and therefore, Gall believed that one should be able to measure a person's abilities to perform different functions by measuring portions of the skull. While in part correct (LeMay, 1976), Gall's hypotheses led to the pseudoscience of phrenology. In the mid-19th century, Paul Broca, a French physician and anthropologist, after listening to a lecture by Auburtin, who was influenced by the work of Gall, had a patient who could, for the most part, say only one word “tan.” After this patient died, Broca removed the brain and found a lesion that was primarily in the left frontal lobe. Subsequently, Broca (1863) described eight patients who were right handed and who had lost their speech from damage to the left hemisphere, thereby supporting Gall's postulate of modularity or localized functions. In regard to Gall's second hypothesis, that bigger is better (i.e., the greater the number of nerve cells and neuronal connectivity in a module, the better this area may be able to carry out its function) was not demonstrated until Geschwind and Levitsky (1968) reported that the area on the left side of the brain that stores the memories of how words sound (i.e., Werncke's area) is larger than the same area on the right side of the brain. It has also been shown that talented musicians have a larger auditory cerebral cortex than do non-musicians, and those with perfect pitch have a larger auditory association cortex on the left than right side of their brains (Schlaug, Jancke, Huang, & Steinmetz, 1995); however, because brain stimulation can alter brain growth, it is not fully clear if this alteration of size is nature or nurture.

Gardner (1985) suggested that people have multiple intelligences. Weisberg (1999) examined the relationship between knowledge and creativity and concluded from this review is that domain-specific knowledge is a prerequisite for creativity; however, there has not been much research to learn how the brains of people who have exceptional creativity are different from healthy controls.

One of the greatest geniuses of the 20th century was Albert Einstein. Although Einstein wished to be cremated, he also wanted his brain to be used for research so that people might be able to learn why he was creative. Einstein died in 1955 and Thomas Stoltz Harvey, the pathologist at the hospital in Princeton, New Jersey, removed Einstein's brain from his skull. Whereas the brain of the patient described by Paul Broca's remains intact and can be viewed in the Museum of Man in Paris, Thomas Harvey sectioned Einstein's brain into about 170 small blocks, made slides from these blocks, and sent it to a variety of people. Fortunately, Harvey did take some photographs before cutting Einstein's brain into these little pieces. Witelson, Kigar, and Harvey (1999) viewed these pictures of Einstein's brain in order to better understand what may have accounted for his genius. They noted that the left Sylvian was shorter in Einstein's brain than in most people. In addition, normally at the posterior end of the Sylvian fissure, there is an upward turning fissure called the ascending ramus which divides a portion of the inferior parietal lobe, called the supramarginal gyrus, into two divisions. This ascending ramus was not present in Einstein's brain. Studies of patients with strokes have revealed that the parietal lobe is critical for performing many functions. Thus, Witelson and colleagues (1999) posited that his left undivided inferior parietal lobe enhanced Einstein's ability to perform the type of computations needed in physics.

The finding that Einstein had a shortened Sylvian fissure and did not have an ascending ramus at the end of his Sylvian fissure may suggest that the growth of his left inferior parietal cortex and left posterior temporal lobe was not as great as those who do have such a fissure. In addition, Marion Diamond and her coinvestigators also found that when compared with the supporting glial cells, Einstein has fewer neurons in his parietal lobe. These left hemispheric abnormalities may have explained Einstein's developmental disorders. His parents brought him to the doctor at the age of 3 because he was not speaking (Hoffman & Dukas, 1972). The posterior portion of the left temporal lobe is important for speech, and Dejerine (1891) demonstrated that lesions of the left parietal lobe can cause an acquired reading disorder (alexia). Kantha (1992) suggested that the abnormalities reported by Diamond, Scheibel, Murphy, and Harvey (1985) in Einstein's left parietal lobe probably accounted for his dyslexia rather than his genius.

There are multiple studies that have revealed that in most people, it is the left hemisphere that primarily mediates language, including speaking and understanding speech as well as reading and writing. In contrast, the right hemisphere appears to be more important for spatial reasoning (Benton, Hannay, & Varney, 1975). Einstein stated that his thinking about scientific problems and developing solutions to these problems was heavily dependent on spatial reasoning and spatial imagination (Metcalfe & Wiebe, 1987). Geschwind and Galaburda (1985) suggested that the delay in development of the left hemisphere which normally mediates language might allow the right hemisphere that mediates spatial reasoning, to become highly specialized. Therefore, it is possible that the abnormal development of Einstein's left hemisphere may have allowed his right hemisphere to become highly specialized for spatial computations.

Partial support of this disinhibition postulate comes from Miller, Boone, Cummings, Read, and Mishkin (2000) reports of several patients who had degeneration of the left frontal and temporal lobes (frontotemporal lobar degeneration) and perhaps as a result of this degenerative disorder developed into wonderful artists. Although Ghacibeh and Heilman (2013) studied epileptic patients who had removal of their left anterior temporal lobe and did not find that this procedure enhanced these participants’ visual creativity, these patients were epileptic and may have had different brain organization than those patients reported by Miller and colleagues (2000). Gansler and colleagues (2011) wanted to learn whether the creative visuospatial performance on the figural Torrance Test of Creative Thinking (TTCT) is associated with measurements of cerebral gray matter volume in the regions of the brain that are thought to be important in for visuospatial processing. High-resolution magnetic resonance imaging scans were acquired, and voxel-based morphometry regression analyses of TTCT to cortical volume were restrained within the anatomic regions identified. The one significant positive focus of association with TTCT emerged within the gray matter of the right parietal lobe. Based on the studies of parietal lobe function and the requirements of the TTCT, the enlarged area normally plays an important role in the mediation of global aspects of attention and visuospatial processing including the capacity for manipulating spatial representations.

Chen and colleagues (2014) studied the relationship between creative achievements and cognitive flexibility using voxel-based morphometry. They found that portions of the dorsolateral frontal lobe and ventral medial prefrontal cortex were larger in those with higher creative achievement. Zhu, Zhang, and Qiu (2013) found that portions of the left inferior frontal lobe were larger in verbally creative people. Takeuchi and colleagues (2010) also found that the dorsolateral frontal lobe (primarily on the right side) was associated with divergent creative cognition. As will be discussed, the lateral frontal lobes are critical for disengagement and divergent reasoning, and these functions are one of the first requirements of creative innovation. Fink and colleagues (2014) reported that verbally creative people have increased gray matter in the left cuneus and precuneus; however, Chamberlain and colleagues (2014) also found in visual artists an increase in gray matter in same area of the brain, but on the right side. Jung and colleagues (2010) measured creativity and performed structural magnetic resonance imaging, analyzing cortical volume. These investigators found that the right posterior cingulate correlated positively with the participants' scores on the composite creativity index. The reason for these results is not entirely clear; however, the cuneus, precuneus, and posterior cingulate are all an important part of the default network (Raichle & Snyder, 2007) and the default network activates when people close their eyes and generate internal thoughts and images. The generation of internal thoughts and images are critical elements of creative innovation.

Nature or Nature in Creativity

Hebb (1949) in his book The Organization of Behavior explained that neurons that fire together wire together, and the acquisition of knowledge and skills is based on alterations of synaptic strengths among the neurons in modular networks. As discussed earlier, the more neurons a person have in a particular network and the greater the branching of the neurons in this network, the more knowledge that this network can store. Thus, a person with high levels of cognitive knowledge in a domain might have more neurons as well as more connections between these neurons in their brain networks that store this knowledge.

Rosenzweig and Bennett (1996) found that rodents who were put in enriched environments at an early age after their maturity could learn more rapidly and store more knowledge than those who were not exposed to this enrichment. When these rodents’ brains were examined, those who received this enrichment had a thicker cerebral cortex. In addition, the cortical neurons in these animals had an increase in the number of dendritic spines. Subsequently, it was revealed that training can alter different parts of the human's cerebral cortex. For example, children who take music lesson from an early age will often reveal a larger auditory cortex than those who had not taken lessons (Schneider et al., 2002). In the domain of music, many of the world's most creative composers grew up in enriched musical environments. For example, Mozart's father was also a composer, as well as a director of a symphony, and a music teacher. Beethoven's father and Chopin's mother were music teachers. In contrast to these composers, who had enriched childhood experiences, children who were put in orphanages, where they received little stimulation, for the most part were found to have very low intelligence and are cognitively disabled (Kaler and Freeman, 1994).

Whereas creativity is heavily dependent on nurture, and this nurturing has the greatest influence during childhood, the child must have genetic and biological capacity (nature) to benefit from being nurtured. In addition, there are many brilliant people who have high IQs, great stores of knowledge, and have been extensively nurtured, but who have not had creative careers. Therefore, the ability to learn and store knowledge (intelligence) and the acquisition of specialized knowledge and skills are all critical components of creativity, but they alone are not entirely sufficient for creative innovation.

Divergent Thinking

Disengagement

There are multiple definitions of creativity, but like the definition of creativity, we provided almost every definition of creativity includes novelty. Therefore, in order to develop new ideas, artistic works, scientific discoveries, and new products, a person must first be able to break away from already accepted theories, ideas, beliefs, practices, and products. This breaking away is called “disengagement.” People, cultures, and religions often encourage stability and discourage or even abhor dramatic changes. Consequently, in many domains, disengagement is often discouraged and even scorned. For example, Galileo, who provided evidence to support the Copernicus heliocentric theory, was punished by the Catholic Church. Finally, in 1992, Pope John Paul II expressed regret for Church's treatment of Galileo and issued a declaration acknowledging the errors committed by the Catholic Church.

Derek Denny-Brown (personal communication) noted that patients and experimental animals with frontal lobe lesions often demonstrated inappropriate approach behaviors, such as a tactile grasp reflex and magnetic apraxia where patients' hands approach viewed objects. In contrast, parietal lesions appear to induce a tactile avoidance response. Based on these observations, Denny-Brown noted that all animals, from amoeba to humans, have two major or basic forms of behavior: they can either approach or avoid. Based on these observations, Denny-Brown and Chambers (1958) proposed that normally the frontal lobes mediate avoidance behaviors and the posterior temporal–parietal lobes mediate approach behaviors. Therefore, when a patient has a frontal lobe injury, he/she will often demonstrate impaired disengagement and abnormal approach behaviors. One of the best examples of abnormal approach behaviors was reported by Lhermitte (1983) who placed objects in front of patients who had frontal lobe injuries. For example, on a table in front of a patient, Professor Lhermitte placed either a pen and paper or an empty glass with a pitcher of water. He noticed that unlike most normal people, these patients, without being asked to use these objects, would start writing or they would pour the water from the pitcher into the glass and drink this water.

Luria (1969) developed some bedside tests to learn whether patients with frontal injury have three different forms of impaired motor disengagement. One test for imitative behaviors called “echopraxia” is the 2-1 Task. In this test, patients are instructed, “When I put up one finger you put up two fingers and when I put up two you put up one.” Patients with frontal lobe dysfunction often echo the examiner and put up the same number of fingers as the examiner, and thus, they cannot disengage from the stimuli they viewed. Another type of disengagement failure is defective response inhibition. We test this by telling patients to put their hands on their laps, close their eyes, and when we touch their left hand, they are to lift their right hand and vice versa (Crucian et al., 2007). Patients with defective respond inhibition will often raise the hand that was touched rather than the opposite hand. The third type of disengagement disorder is perseveration where a person continues performing the same action when a different action is needed. Perseveration can be continuous or recurrent. One of the simplest tests for this is to ask patients to write a series of alternating M and Ns (i.e., mnmnmnmnmn). Patients with perseveration will often repeat one of the letters (e.g., mnmnmnmmmmm).

These tests of disengagement examine motor planning and actions, but there are also neuropsychological tests that assess for cognitive disengagement. One such test is the Stroop, where people have to disengage from reading words that denote colors and instead name the color of the font in which this word was printed and this font is often a different color than denoted by the written word.

Whereas disengagement is a critical element of creativity, disengagement alone does not lead to innovation. Thus, a critical element of creativity after disengaging is the development of ideas that are different from the prevailing modes of thought and expression. Some people call this form of reasoning, “thinking out of box.”

Zangwell (1966) posited that because the frontal lobes are critical for divergent thinking, frontal lobe dysfunction could disrupt divergent thinking. In 1948, Berg developed the Wisconsin Card Sorting test where participants are provided with a deck of cards and these cards have several different shaped figures, with several colors, different sizes, and several different number of these figures on these cards. The participant's task is to sort these cards based on one of these characteristics, until the examiner no longer agrees with this sorting strategy and then the participant must determine a new sorting strategy. Milner (1963) demonstrated that intractable epileptic patients whose seizures emanated from their frontal lobes, and as a treatment had these portions of their frontal lobes surgically removed, often failed to alter their sorting strategy, providing support for Zangwell' s hypothesis that the frontal lobes are critical for the ability to perform divergent thinking. Functional imaging studies provided additional support for this divergent thinking hypothesis (Weinberger, Berman, & Zee, 1986).

One of the tests often used to assess divergent thinking is the Alternative Uses Test (Guilford, 1967). The participant is told that the examiner will verbally provide a common object such as a “brick” and that in 3min, he or she is to give as many novel uses for this object as they can. The participants are also told that they will be scored for fluency and novelty. For example, if the participant states a common use of this object (e.g., build houses), they will receive a score of 1 point for this response. If they provide a somewhat unusual response (e.g., used as a door stop), they get a score of 2 points, and if highly unusual (e.g., use it in the bath tub to remove calluses from their feet), they get 3 points. The full score is the sum of the points which indicates a combination of this participant's fluency and novelty. Using functional imaging, it has been reported that when creative subjects are providing alternative uses of bricks, their frontal lobes showed more activation than those who were less creative (Carlsson, Wendt, & Risberg, 2000).

Another test commonly used is the abbreviated or brief TTCT (Torrance, 1974). This test has both a verbal and a visuospatial subtest. In the verbal test, the participant is given a scenario (e.g., there is a severe fog where people can only see other people's feet) and the participants are asked to tell a story based on this scenario. In the visuospatial part of this test, the participants are presented with some curved lines and asked to draw a picture based on these lines.

It is not entirely known why the prefrontal lobes play such an important role in divergent thinking. Knowledge about the use of objects such as a brick are stored in semantic networks that are located in the temporal and parietal lobes. Based on the Hebbian concept of neurons that fire together wire together, the semantic networks that store the most common uses of objects (e.g., build houses) should be the strongest and easiest to activate. When performing divergent thinking, a person has to disengage from these strong networks and activate more remote networks. The frontal lobes have strong connections with the portions of the temporal and parietal lobes that store information (Pandya & Kuypers, 1969), and the frontal lobes may facilitate activation of these more remote networks. Although it is not entirely known how the frontal lobes facilitate the activation of these more remote networks, the frontal lobes are one of the few areas of the cerebral cortex that appears to control the activity of the locus coeruleus (Arnsten & Goldman-Rakic, 1984) which produces norepinephrine for the brain, and as will be discussed in a subsequent section, the level of norepinephrine in portions of the brain may influence the activation of remote networks.

Novelty Seeking

Highly creative people are more than curious. Curious people do search and discover, but creative people are discovering and also developing that which is new and different. They are novelty seekers. When having a novel-creative thought, having discovered something new or produced a creative product, people often get feeling of deep joy and excitement, the “Ah Ha” or “Eureka!” experience. The great composer Pyotr Ilyich Tchaikovsky stated “… It would be vain to put into words that immeasurable sense of bliss which comes over me … (when) a new idea awakens in me … .” Many drugs, such as cocaine, can also induce a sense of bliss and many creative people, especially writers, composer-musicians, and fine artists, have a very high rate of substance abuse (Post, 1994, 1996). A creativity study that compared the students who have used drugs with those who have not used drugs suggested that the students who used drugs tended to be more creative (Eisenman, Grossman, & Goldstein, 1980). One possible explanation for this relationship is by some manner these drugs enhance creative performance; however, studies of creativity under intoxicated states do not reveal that drugs enhance creativity (Lang, Verret, & Watt, 1984; Lapp, Collins, & Izzo, 1994). Cecil B. DeMille, a film producer as well as a director and one of the fathers of the Hollywood cinema, stated that “Creativity is a drug I cannot live without.” An alternate hypothesis is that the same brain network that produce a sense of bliss in response to some drugs also produces the deep joy and excitement during the “Eureka” experience.

Olds and Milner (1954) inserted electrodes into the septal nucleus of rats. When these rats pressed a lever, these electrodes activated the septal region. This stimulation was so rewarding to these rats that they continued to press this lever until they were exhausted. Stimulation of the ventral tegmental area that contains dopamine neurons that project to the nucleus accumbens by means of the mesolimbic pathway has also been found to be rewarding. The nucleus accumbens is connected with the ventral striatal system and functional imaging studies suggest that this ventral striatal system becomes active during reward. Patients with Parkinson's disease have a loss of the neurons that manufacture the neurotransmitter dopamine. Patients with Parkinson's disease are often treated with medications called dopamine agonists, which increase the brain's sensitivity to dopamine. Clinicians have reported that one of the complications of this dopamine agonist treatment is that with this treatment, several Parkinson patients who took one of these medications became high-risk takers. There is some evidence that exposure to novelty also activates the mesolimbic dopamine system of the brain (Bardo, Donohew, & Harrington, 1996), and it is this same neural system that mediates the rewarding effects of drugs of abuse. These observations suggest that like drugs of abuse, novelty, discovery, and creativity can excite this ventral striatal reward system. Support for this hypothesis comes from recent reports by Lhommée and colleagues (2014) and Faust-Socher, Kenett, Cohen, Hassin-Baer, and Inzelberg (2014) who demonstrated that patients with Parkinson's disease, who were receiving dopamine agonist treatment, had enhanced creative thinking.

Associative and Convergent Thinking

Corpus Callosum

In the beginning of this article, creativity was defined as the new discovery, understanding, development, and expression of novel orderly relationships, or metaphorically, “finding the thread that unites.” James (1890) suggested that creativity requires an “… unheard of combination of elements and the subtlest associations … .” Spearman (1930) suggested that creative ideas result from the combination of two or more ideas that have been previously isolated. As mentioned earlier, because the reports of Paul Broca we have had increasing evidence that the human brain is organized in a modular fashion, and therefore, creativity often requires that there be communication between modules. The right and left hemisphere store many different forms of information and many creative works require interhemispheric communication. For example, the left hemisphere mediates mathematical calculations, but the right hemisphere appears to be important in spatial cognition (Benton et al., 1975), including spatial imagery (Butters, Barton, & Brody, 1970). Thus, the creative physicist may have to use both hemispheres when developing new theories. Liepmann (1920) demonstrated that in right-handed people, the programing of skilled movements is mediated primarily by the left hemisphere, but as mentioned, the right hemisphere is dominant for mediating spatial relationships, and therefore, the artist when planning and painting must often also use both hemispheres. In addition, when painting, the artist has to focus on the object being painted; however, the artist also has to be aware of how this object integrates with other objects in the painting. It has been demonstrated that whereas the left hemisphere mediates focused attention, the right mediates global attention (Barrett, Beversdorf, Crucian, & Heilman, 1998; Kosslyn, 1998; Robertson, Lamb, & Knight, 1988), and thus, creation of great painting requires the coordination of both hemispheres. Even when composing music, there has to be interhemispheric integration because the right hemisphere is important for processing melody and the left hemisphere processes rhythm (Gates & Bradshaw, 1977).

There are many more examples of how interhemispheric communication is critical in the creative process. The structure connecting the modular systems in the right and left hemisphere is the corpus callosum. One of the tests used to assess creativity is the Inkblot or Rorschach test. There are some patients who had seizures that spread from one hemisphere to the other and anti-seizure medications could not successfully control these patients' seizures. To prevent the interhemispheric spread of seizures, neurosurgeons cut the corpus callosum. Lewis (1979) administered the Rorschach test to eight patients before and after they had undergone a cerebral commissurotomy, and assessed the creativity of their verbal responses. After these patients had their commissurotomy, there was a reduction in their creativity on this Inkblot task. The right hemisphere plays a dominant role in the mediation of visuospatial perception and global visual attention and the left hemisphere mediates speech. Therefore, severing the connections between the two hemispheres that mediate these cognitive activities impaired these patients creativity. Mednick (1962) noted that when generating associative responses to a stimulus, creative individuals are characterized by the ability to activate highly distributed semantic-conceptual networks. Based on observations such as that reported by Lewis (1979), Bogen and Bogen (1988) suggested that it is also the suspension of the independence of cognitive networks that accounts for creative innovation. Support for Mednick's (1962) theory (that creative innovation is related to the recruitment and interaction of different networks) comes from electroencephalographic (EEG) studies of normal subjects who, during creative thought, demonstrated an increase of anatomically distributed coherence of EEG oscillations (Jausovec & Jausovec, 2000; Petsche, 1996). In other words, this EEG study suggests that during creative cognition, there appears to be physiological evidence that the brain is “finding the thread that unites.”

Whereas the exact mechanism accounting for the wide spread coactivation of modulating coactivation of brain networks is not fully known, the next section of this article discusses several possible mechanisms that may account for widely distributed coactivation and integration of cognitive networks.

Modulating Coactivation of Brain Networks

Incubation

Many people who are attempting to find solutions for a problem that they could not initially solve, when either working on other problems or performing some other form of cognitive activity, suddenly become aware of a solution. People often call this the “Ah-Ha” or “Eureka” experience. Both Helmholtz (1826, as cited in Eysenck, 1995) and later Wallas (1926) suggested that an important stage of creativity is incubation, the nonconscious process of problem solving. Dijksterhuis and Nordgren (2006) performed several studies that examined the insight induced by nonconscious (incubation) versus conscious thought. For example, participants were to select a new house from two choices and each house had different attributes. These investigators found that a period of distraction where the participants could not consciously think about this decision often led to better decisions than conscious thinking. Many people who cannot make a decision will often say, “Let me think about it.” However, for the most part, these people get busy with other activities and then they often “come up with” the best decision. Whereas a diversion of thought with nonconscious thinking may lead to creative ideas and the “Ah-Ha” experience, the brain mechanisms that can account for this nonconscious insight remain to be determined. On the other hand, many creative ideas are also developed during conscious problem solving.

Sleep

One of the most famous stories about creativity and sleep is that of August Kekule. Many creative people have noted that they developed insight into a difficult problem or have creative thoughts when they were either falling asleep or awakening from sleep. Although there is a lot of debate about the veracity of this story, one of the best known examples of the relation between sleep and creativity is the story of August Kekule. Whereas chemists knew that benzene had six carbon atoms, it was unknown how the atoms were spatially organized. In 1865, either during sleep or while in a sleepy state, Kekule dreamed of a snake chasing its tail, making a ring. This dream provided Kekule with the idea that benzene has a ring-like structure. Dehaene (1997) mentions in his book called The Number Sense that many mathematical geniuses have claimed that they have had some of their most creative moments during sleep.

The brain mechanisms by which sleep aids creativity is not fully understood. Drago and colleagues (2014) performed one of the first studies attempting to understand this relationship and noted that there are several different physiologic states associated with sleep. There are both rapid eye movement (REM) sleep and non-rapid eye movement (NREM) sleep, and NREM sleep can be broken down into Stages (1–4). Each of these stages is characterized by the degree of EEG slow-wave activity. During NREM sleep, there are also cyclic alternating patterns (CAPs) of EEG activity, and based on the frequency of the EEG waves, these CAPs can also be divided into three subtypes (A1–A3). Drago and colleagues wanted to learn the relationship between CAP activity during sleep and creativity. They studied healthy young adults by performing polysomnographic recording on three consecutive nights. On the second and third mornings after these recording, these participants were tested with the Abbreviated TTCT. The results indicated that the amount of several stages of NREM sleep correlated with creativity. In addition, there was a negative correlation between creativity and the extent of REM sleep. The reasons that NREM sleep is associated with higher levels of creativity are not fully known; however, NREM sleep is associated with low levels of cortical arousal, and as will be discussed below, low cortical arousal may enhance the ability of people to access their more remote associations that is often critical for creative innovation.

Rest and Relaxation

The founder of the nerve theory and a Nobel Prize winner, Ramon y Cajal (1897), wrote a book entitled Advice for a Young Investigator. In this book, he provided some advice about developing a creative solution, “If a solution fails to appear after all of this, and yet we feel success is just around the corner, try resting for a while. Several weeks of relaxation and quiet in the countryside brings calmness and clarity of the mind. Like the early morning frost, this intellectual refreshment withers the parasitic and nasty vegetation that smothers the good seed. Bursting forth at last is the flower of truth, whose calyx usually opens after a long and profound sleep at dawn-in those placid hours of the morning that Goethe and so many others consider especially favorable for discovery.”

Kuhn (1996) in his important book The Structure of Scientific Revolutions called a great change in scientific thinking a “paradigmatic shift.” Some of the greatest paradigmatic shifts in the modern error include Einstein's theory of relativity, Mendel's hereditary theory with the development of the science of genetics, Darwin's theory of evolution, and Newton's development of calculus and theory of gravity. Although each of these paradigmatic shifts had a different influence on science, these great scientific revolutions all came about while these scientists were in a similar psychological state. Darwin was taking a cruise on the Beagle. Einstein worked 8 hr a day in the patent office, but following his work, he remained in the office and work late at night. Sir Isaac Newton who was working at Cambridge University had to leave when the University closed because of an epidemic of the bubonic plague. Newton went to his mother's farm and while relaxing at the farm (under a tree so it is told) developed the law of gravitation as well as calculus. Gregor Mendel was gardening sweet peas at his monastery when he developed the hereditary-genetic theory. All these paradigmatic shifts occurred during the times these creative people were relaxing.

Depression

Kraepelin in 1921 was perhaps the first to note that manic-depressive psychosis was often associated with enhanced creativity (Weisberg, 1994) and several investigators have reported that many of our most creative writers, composers, painters, and scientists have suffered with depression, either bipolar or monopolar (Andreasen & Glick, 1988; Poldinger, 1986; Post, 1994; Richards, Kinney, Lunde, Benet, & Merzel, 1988; Slaby, 1992). Andreasen and Glick (1988) noted that during severe depression, it is unusual for creative people to be productive, but noted that Pickering (1974) has thought the these periods of illness may be useful to creative individuals, in that they may provide an incubation period in which ideas may be developed.

The reason why relaxation and depression often appears to lead to creative innovation is not entirely known; however, Easterbrook (1959) posited that high levels of cortical arousal induced by stress might in some manner inhibit or suppress the emergence of remote associations. In contrast, lower degrees of cortical arousal may allow unusual associations to become manifest. As mentioned earlier, the activation of remote associations is a very important aspect of innovation. But why does a lower degree of cortical arousal alter the activation of remote associations?

Norepinephrine

Norepinephrine is one of the brain's most important neurotransmitters and has a critical role in modulating the brain's arousal. Thus, the thread that may unite creativity with depression, resting or relaxing, and sleep-dreaming are the alterations in the level of this neurotransmitter (McCarley, 1982).

Psychological stress has been shown to be associated with higher levels of norepinephrine and relaxation with lower levels. It is thought that depression may be induced by a reduction in the brain of both norepinephrine and serotonin. This theory is supported by the observations that one of the most successful treatments for a major depressive disorder is the use of medications called serotonin–norepinephrine reuptake inhibitors that increase the level of these two neurotransmitters in the brain.

The Remote Associates Test is a creativity test developed by Mednick (1962), which is used to determine a person's creative potential. When performing this test, the participant is presented with three common words (e.g., American, blue, and goat) that appear to be unrelated and the participant is requested to produce a fourth word that is related to each of the first three words (e.g., cheese). This test was designed to assess peoples' ability to activate-access remotely connected lexical-semantic networks. If subjects are put under stress conditions when taking this test (state anxiety), their performance deteriorates (Martindale & Greenough, 1973). Stress increases the activity of the noradrenergic (norepinephrine) system and norepinephrine alters the brains signal-to-noise-ratio by suppressing intrinsic excitatory synaptic potentials relative to the potentials elicited by direct (external) afferent input (Hasselmo, Linster, Patil, Ma, & Cekic 1997). This change of activity induced by norepinephrine biases the brain toward external stimuli that may be important for “flight or fight” activities; however, creative ideas are produced by looking “inside” and norepinephrine inhibits the ability of a person to “look inside” as well as contracting the widespread networks that are so important for creative innovation.

The Scholastic Aptitude Test (SAT) has questions that can be answered with crystalized knowledge, and also contains questions that require reasoning. Students who have severe anxiety when taking this test often perform more poorly than expected based on their academic performance. The questions with which these anxious students had the most difficulty were those that required reasoning skills, rather than those that required crystalized knowledge; however, when these students took propranolol immediately before taking the SAT, their scores improved (Faigel, 1991). Propranolol blocks the action of norepinephrine on the brain, and this blocking might have allowed these students to enlarge their semantic networks as well as increase their cognitive flexibility.

We wanted to test the hypothesis that propranolol, which blocks the influence of norepinephrine, would enhance cognitive flexibility, and thereby allow a person taking this medication “to find the thread that unites”. We tested normal participants' ability to solve anagrams when treated with either ephedrine or propranolol. Our results revealed that these healthy participants performed better when they had taken propranolol before performing this task.

The neurons that manufacture norepinephrine are found in the midbrain nucleus coeruleus. The vagus nerve carries information from the viscera to brain and activation of the vagus nerve can activate the locus coeruleus which will increase the production of norepinephrine in the brain. Stimulation of the vagus nerve can be used to treat epilepsy, when other measures have failed. We measured the creativity of patients who were being treated with vagal nerve stimulation, during the time they were being stimulated and also when they were not being stimulated (Ghacibeh, Shenker, Shenal, Uthman, & Heilman, 2006). To assess creativity, we used the TTCT, and to assess cognitive flexibility, we used an anagram test. The participants did not know whether or not they were being stimulated. We found that during stimulation, there was a reduction of cognitive flexibility and a reduction of creativity. The results of this study provided additional support for the hypothesis that cognitive flexibility and creative thinking are related to the reduced activity in the locus coeruleus. It would appear that increased activity of brain's adrenergic system, which increases the brain's signal-to-noise ratio and improves the brain's ability to attend to sensory input, also decreases its ability to recruit large-scale networks.

As we mentioned earlier, people appear to be more creative during the times they are in a relaxed state than during the times they are under much stress. Typically, when an EEG is performed on a person who is awake, but in relaxed state, this EEG will often demonstrate alpha activity (brain waves that occur 8–12 cycles per second). With stress and high arousal, this alpha activity abates and people develop higher frequency waves on their EEG. Berridge and Foote (1991) provided evidence that activation of the locus coeruleus alters the brain waves as recorded on an EEG from slower alpha activity to more rapid activity. Martindale and Hasenfus (1978) examined their participants' ability to write creative stories. Based on the creativity of these stories, these participants were placed into either the creative or uncreative group. These investigators also recorded these participants' EEG both when they were resting and when they were writing stories. Analysis of these EEGs revealed that in the resting state, there were no differences between these two groups; however, during the time they were developing their stories (“innovation stage”), the creative subjects had significantly better developed alpha activity than did the less creative subjects. These results provide physiological support for the postulate that maintaining a low level of arousal enhances creative innovation.

As noted earlier, many people with a history of depression or bipolar disorders have been found to be creative, and the observation that patients with depression often respond to medications which increase brain norepinephrine (Delgado and Moreno, 2000) provides indirect evidence that levels of arousal mediated by norepinephrine may influence creativity. Further support for this hypothesis comes from studies of arousal in people with depression. Using EEG power analysis, it has been shown that people with depression have reduced arousal, and this reduced level of arousal is reversed with treatment (Knott, Mahoney, & Evans, 2000; Nieber & Schlegel, 1992).

Closing Comments

Creativity is one of humans' most important activities, and a cherished gift, but of all our behavioral abilities, it is one of the least investigated. Not only do we need to better understand the brain mechanisms that may mediate creative activities in multiple domains, but we also need to learn how we can optimize creativity. Aging, neurological, and psychiatric diseases may have important influences on creativity, and thus, we also need to learn how aging and diseases influence the different aspects of creativity and what can be done to treat these disorders. Currently, although neuropsychologists and neurologists assess many different cognitive functions (e.g., episodic memory, language, calculations, working memory, executive functions, sensory perception, and intelligence), it is rare for the clinician to test for creativity. Although there are tests that can assess elements of creativity such as disengagement (Stroop Test, Wisconsin Card Sorting), divergent thinking (Alternative Uses, Torrance Test), and convergent thinking (Mednick's Remote Associates Test), some of these tests are rarely used to evaluate patients. In addition, there is a great need to further develop tests of creativity. Finally, we know that stimulation during childhood enhances cognition and even can alter the brain both anatomically and physiologically, but we need to learn more about what could be done to enhance children's development of creativity.

Conflict of Interest

None declared.

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