GREENBERG (2002) The Beast at Play: the Neuroethology of Creativity (ANNOTATED)

Preprint—to be published in

The Child’s Right to Play: A Global Approach

Rhonda Clements & Leah Fiorentino, editors

 Praeger/Greenwood Press, Westport CT

2002

 The Beast at Play: the Neuroethology of Creativity

Neil Greenberg

https://neilgreenberg.com/greenberg-2002-the-beast-at-play-the-neuroethology-of-creativity/ 

ANNOTATED for Art & Organism seminar, 2020

The philosopher, Eric Hoffer once said, “It is the child in man that is the source of his uniqueness and creativeness, and the playground is the optimal milieu for the unfolding of his capacities and talents.”  The ideal university, like the research laboratory and the artist’s studio, should have much in common with the playground.

Our understanding of the development and expression of creativity will profit from the critical scrutiny of biology.  Creativity can be viewed as a fundamental behavioral trait that is grounded in the basic biology of the brain.  Further, it has likely evolved under the influence of the physiological stress response, originally designed to help organisms cope with challenges to their stability.  As such, the capacity to recognize and deal with novelty and change are driving forces.  Art can be construed as an extreme example of creativity capable of engendering insight into one’s self and others.  Depending on who those others might be, we may speak of artists with varying measures of skill, specific constituencies, or even very limited audiences—the “artist’s artist.” [or the artists whose audience is one’s self]  As such, art is a form of communication (“a bridge linking the painter’s mind with that of the viewer,” said Eugene Delacroix).  But like all communications, it may also constitute an important bridge between different parts of artist’s mind (C.D. Lewis wrote, “We do not write in order to be understood; we write in order to understand”).  Thus, while one’s creative gifts are known by the breadth or depth of their capacity to communicate, effective communications can also feed back into one’s personal development.  Indeed, this may be a key to the therapeutic and self-actualizing dimension of art and creative experience.  In his seminal Psychoanalytic Explorations in Art, Ernst Kris (1952) outlined how the dual processes of primary and secondary processes of mind are put in the service of creativity and art.  As communications, he noted, art serves in two ways—one in which the id communicates with the ego and one in which its processes are submitted to others (p 61)                

Creativity is central to a full understanding of both play and art [and science].  This apparently innocent assertion implies a deep continuity between these activities as well as the position that creativity is present by degrees in all humans and not a characteristic of unusual individuals with rare conjugations of highly developed abilities.  And the intent to view these behavioral patterns from the ethological perspective reveals a conviction that they are also present by degrees in related species.  Creative activities have come to possess their present form by the kinds of processes that have guided the emergence of other adaptive traits from unexpected beginnings in their evolutionary ancestors.

CREATIVITY DEFINED

AA definition,” Samuel Butler once said, “is the enclosing a wilderness of ideas within a wall of words,” but as Joseph Campbell (1968) cautioned, “The best things can’t be told . . .”   And to bring order to the chaotic wilderness of ideas about creativity is in itself a major creative undertaking.  The formidable Council of Scholars of The Library of Congress assembled when Daniel Boorstin was Librarian sought to “rescue” the term “for use in the world of ideas and culture” (Hutson 1981).  While they agreed that “innovation” was at its core, they also argued that for innovation to be creative, in must be “important.”  The 28 Scholars sought to reclaim “creativity” from trivial applications such as “preschoolers’ finger painting.”  I am also seeking a central essence for creativity and seeking to reclaim this behavioral pattern as a suitable subject for ethology, that unique multidisciplinary field in which biology and comparative psychology collaborate in seeking to understand the causes and consequences of behavior.  Creativity is a trait of living organisms and must be made amenable to the development of predictive, testable hypotheses about its underlying biological causation and control if it is to be understood.

Traditional definitions of creativity.  Etymology can be instructive, often revealing unexpected implicit biases based in language.  The Random House Dictionary of the English Language (1987) and the Merriam-Webster’s Dictionary on-line identify “create” as verb rooted in Middle English, from Latin creatus, past participle of creare; akin to Latin crescere to grow, also, to originate or invent,  from at least the 14th century.  In its transitive senses it means first Ato cause to come into being, as something unique that would not naturally evolve or that is not made by ordinary processes” — to bring into existence as in, “God created the heaven and the earth” (Gen 1:1; Authorized Version).  It is also the cause or occasion of a phenomenon, as in “famine creates high food prices.”  A later definition deals with the sense most familiar to scholars: “to produce through imaginative skill, as in “create a painting,” that is “to evolve from one’s own thought or imagination, as a work of art or an invention.” or  “to cause to happen; bring about; arrange, as by intention or design—or to design, as to “create dresses” or to create a revolution or an opportunity to (e.g.) ask for a raise.  In its intransitive senses,  to make or bring into existence something new.   Creativity used to be regarded less as an intrinsic human capacity than as theophany—a “manifestation of a transcendent deity who inspired the work and whose glory was expressed within it” (Novitz 1987).  The influence of that perspective lingers.

Evolution: Needs and Coping, Adaption and Fitness.  To make the idea of creativity more accessible to biology, I must argue that it is an adaptive biological trait. [this may seem evident, depending on the level of organization at which you consider it, but it has been and is still often considered as a function of transcendent influences]  As an adjective, “adaptative” refers to a demonstrable contribution to fitness.  The great virtue of defining creativity as an evolved biological phenomenon is that the insights and methods of biology can be brought to bear in ways that can better illuminate its causes and consequences for the organisms expressing it.  “Adaptationism” harnesses the common (and commonly misguided) assumption that extant traits in organisms have come about because they necessarily  enhance the fitness of the organism that manifests them.  It is true that enhanced fitness describes the central dimension in the selection process that results in one organism or group of organisms prevailing over another in evolutionary time, but the path by which the present condition is attained is not usually obvious and may require an understanding of environmental selective forces that no longer exist.  In this sense, an adaptationist explanation is an hypothesis—a plausible rationale awaiting confirmation.  The contribution of creative behavior to fitness is not necessarily obvious in many of its most extreme expressions, but extreme positions generally represent a tail-end of a continuum that is manifest in a relatively small part of a population, while natural selection generally occurs mainly in the larger population manifesting less extreme expressions.  Unusual members of the population typically prevail in unusual times.  

Creativity is a potent biological adaptation in that it catalyzes or facilitates a regulatory or advantageous change in response to a real or perceived stress by an individual or group of individuals.   Characteristic of adaptative traits is their tendency compensate for or to allow the organism to compensate for change, to preserve stability, the status quo.  This fundamental conservatism of organisms was termed “Romer’s Rule” by the anthropologists Hockett and Ascher (1964), “the initial survival value of a favorable innovation is conservative, in that it renders possible the maintenance of a traditional way of life in the face of changed circumstance” (p.137).  Fitness involves contributions to future generations in terms of one’s own offspring (direct fitness) or those of non-descendent kin (such as siblings, indirect fitness).  “Inclusive” fitness is the combination of these two kinds of contributions to the future (Hamilton 1964).   Usually the contribution is conceptualized in genetic terms, but the relentless logic of evolution requires only that information is reliably transmitted across generations, thus opening the way to conceptualize evolution in cultural terms also.  In the spirit of investigating creativity as an adaptive trait, we can define it thus: 

“Creativity involves both the process and product of unprecedented or novel perception, thoughts, or actions by which an organism or group of organisms copes with present or potential changes in the composition and structure of its environment.  In particular, it manifests an enhanced intensity of perception, cognition, and expression that occurs either spontaneously or is elicited by specific stimuli to relate and integrate variables not ordinarily associated with each other. (adapted from Greenberg 1998)

This definition effectively incorporates and enlarges Poincaré’s (1913) famous definition: “To create consists of making new combinations of associative elements which are useful.” (p. 286)  Creative perceptions, thoughts, or actions within individuals will associate familiar or novel stimuli in varying combinations to help that individual meet its needs, which may be of varying urgency (Maslow, 1954).  Intrinsic reward systems operate to maintain this valuable activity.  When these perceptions, thoughts, or actions are communicated by setting an example (modeling) or by pedagogy (teaching) to serve social needs, the creative individual is identified and acknowledged. 

      A key corollary of a biological approach informed by modern evolutionary theory is that many traits have come to have their adaptive function by being transformed in the evolutionary process from something else. [Indeed, the evolutionary precursors of a trait now recognized as adaptive can often be traced in its evolutionary lineage to a trivial or incidental by-product or side-effect of a trait of much more significance in a different ancestral environment that has little resemblance to the contemporary umwelt—exemplified in striking forms by the process of ritualization. Described in more detail below]  Advantageous modifications of morphology or physiology, however slight between generations can, when subject to natural selection, eventually lead to organs or systems so transformed as to be unrecognizable except by careful systematic study. Here evolutionary biology points out the various kinds of changes in size, shape, timing, or control of a trait that converging internal (genetic) and external (environmental) stimuli might have on its expression.  We can be confident that evolutionary change has occurred when a thread of descent can be demonstrated by comparing related species.  The path from a mouse’s forelimb to the wing of a bat, or from the thermoregulatory feather fluffing of a sparrow to the spreading of a courting peacock’s tail can be viewed as homologous—fundamentally similar even if dissimilar in function.   To apply this corollary to creativity as an evolved behavioral pattern we would have look at what it has in common with traits observed in related species that are likely precursors to the organism we are studying.  When several lines of evidence converge on defending the hypothesis that a specific trait we are studying is much like one in a related species, we can be confident that evolution has occurred.           

Treating creativity as a rare trait, as Martindale (1999) does in his essay, “Biological Bases of Creativity,” makes it more difficult to study by obscuring related traits with which it may form an evolutionary continuum.  Although constructed of several common traits, the necessary conjunction of all of them in the same person is … in Martindale’s view, rare.  But he also employs Poincaré’s famous definition of creativity, mentioned earlier, including his observation that new combinations can “reveal to us unsuspected kinships between other facts well known but wrongly believed to be strangers to one another” (Poincaré, 1913, cited by Martindale, 1999, p.37).  But the discovery or invention of new combinations isn’t rare, it’s the essence of education.  It appears to be a spontaneous process to a point, but is facilitated by the mediation of a “more knowledgeable other.”  Such a person, or the internalized voice of that person, leads the learner or creator to the brink of insight, no matter how modest, but only the person can actually make the connection.  And many connections involve quite complex constellations of ideas that no amount of mediation can facilitate—here is where further communications fail.  As I mentioned above, “The best things cannot be told, the second best are misunderstood.  After that comes civilized conversation …” (Campbell 1968)  

Art itself.   Works of art are conspicuous expressions of creativity that are particularly effective at communicating.  What is commonly called art is often more clearly identified as a work of art –the artifact of the creative process and the principle way in which it is known.  As Coomaraswamy famously put it, Athe words artifact and artificial imply … the thing made is a work of art, made by art, but not itself art; the art remains in the artist and is the knowledge by which things are made” (1956, p.18).  Art is recognized by its capacity to communicate and thereby evoke an enlarged consciousness of some potentially relevant aspect of one’s self, one’s relationship to others, one’s environment.  It is aesthetic because it does this by means of the senses and can also evoke more or less intense experiences of growth and change, the most extreme of which are epiphanous aesthetic experiences, transformative personal insights that can serve one’s needs and perhaps enhance one’s fitness.

Play and art.   Play and art, while often perceived as functionally related to each other,  are also often seen as a luxury, apparently irrelevant to the urgent needs of everyday survival.  In Konrad Lorenz’s (1971) term, autotelic, meaning that they exist only for themselves, they are “self-justifying.”  Lorenz also saw play as a source of deep aesthetic value attributable to its economy of energy and harmony of impulses.  As Gordon Burghardt (1999) points out, apparent purposelessness was long part of the most accepted definition of play.  Artists that sense that complete freedom of expression is central to true creativity frequently demand respect for art for its own sake.  Many view true freedom as necessarily detached from function, or at least current utility.  Certainly, not all functions are obvious, or even extant—we can only speculate about the original function of many contemporary traits that were forged in an ancestral environment. 

      Play is generally assumed to be pleasurable.  Sigmund Freud believed that pleasures are never abandoned, they are replaced by other pleasures.  In normal adults, Freud believed, daydreams replaced play, but in artists, apparently, play was replaced by artistic creativity.  Ellen Winner (1982) points out the thread here that weaves from play through daydreaming and productive work—with passes through neurosis and dreaming along the way. These are all energized, says Freud, by unsatisfied desires, unfulfilled wishes.

Ellen Dissanayake (1992) explored the relationship of art to play in Homo Aesthetics where she comments on “Play theories of art” associated with Friedrich Schiller , Herbert Spencer, Sigmund Freud, and Johan Huizinga (1949).  Desmond Morris (1962), in The Biology of Art suggested that art has been derived from play and exploration; Richard Alexander (1989) derives the human psyche (including art) from “scenario building” that evolved from play.  Dissanayake (1992) emphasizes Amaking special” as a litmus test of art (p. 95),  a quality of a stimulus that can evoke a different and more intrinsically rewarding constellation of neurological activations than can the mundane.   The most complete evaluation of the comparative approach to play is Gordon Burghardt’s (2001) review in which play or play-like behavior is identified in many species.  This helps establish the idea of evolutionary continuity but also underscores its adaptive significance by relating it to ecological and physiological variables.  

Art is arguably derived from play, and certainly science is also.  Our candidate for an archetypal player might be Sir Isaac Newton, who characterized himself in the midst of his search for the truths of science as “a boy playing on the sea‑shore” who diverted himself from time to time with a smoother pebble or a prettier shell.

In a Mark Twain (1903) novel, Tom Sawyer’s view that “Work consists of whatever a body is obliged to do, and play consists of whatever a body is not obliged to do,” (p. 33) is consistent with a traditional view of play as somehow “irrelevant” to the survival of an animal, but this is not likely.  Although the association of play with creative art and science has been made since research on play began, insight must await advances in the biology of cognition, breakthroughs which may emerge from studies of animal play (Fagan, 1981).  When play is defined, as Klopfer (1970) did, as a kind of exploratory activity “by which the organism ‘tests’ different proprioceptive patterns for their goodness of fit” (p. 420), we can accept his thesis that even thought and abstraction is play:  “Perhaps certain patterns of cortical activity do produce behavior of selective value … behavior that is harmonious with the … features of the universe in which we share.  Abstractions may be the play through which we learn how to think well” (p. 403). 

Play is serious.  As Freud pointed out in “Creative Writers and Day‑Dreaming,” the opposite of play is not the serious but the real.  Might we approach reality more closely in the most perfectly polarized play of pure imagination?

Generically, all the discoveries and innovations of  pure science and fine art—those intellectual and aesthetic pursuits which are carried on without reference  to technology or utility—may be credited to functioning of the human play impulses … They rest on the play impulse, which is connected with growth but is dissociated  from preservation, comfort, or utility, and which in science and art is translated into the realm of imagination, abstraction, relations, and sensuous form.  (Kroeber, 1948).

Play was associated with education by Plato (for example Krentz, 1998) and with the discharge of emotions (catharsis) by Aristotle (1962).   In Eros and Civilization, Marcuse  (1955) outlined Schiller’s view that the play impulse mediates the conflict between intuition/sensuousness and cognition/reason.  The play impulse allows man to reconcile feelings and affections with the laws of reason (Chap. 9).  It is also the source of creativity in so far as Anew forms of realization and of discovering the world” will be attained…” (p 204).   The truths of sensuousness are the content of aesthetics and its function is the perfection of sensitive cognition.  “Here the step is made that transforms aesthetics, the science of sensuousness, into the science of art …”   Art which  “challenges the prevailing principle of reason:  in representing the order of sensuousness, it invokes a tabooed logic—the logic of gratification as against that of repression.” 

The “perfection of sensitive cognition” must surely involve what have been termed the primary and secondary processes of cognition.  The revelation of “unsuspected kinships” between ideas recalls the primary process cognition of dreaming, reverie, psychosis and secondary process cognition involving the “abstract, logical, reality-oriented thought of waking consciousness” (Fromm,1978, cited by Martindale, 1999 p.138).  There is an assortment of support for the idea that creative individuals can more easily shift gears from primary process, unfocused attention (associated with low levels of cortical arousal), to a more focused secondary process (higher levels of cortical arousal) for the expression or implementation of creative insights.  This “dual processing” viewpoint, evokes Ernst Kris’s idea of “regression in service to the ego.”  The reservoir of free associations of the primary processes are utilized but reined in by the secondary (Kris 1952).

THE NEUROETHOLOGY OF CREATIVITY

Our working definition of creativity is packed with ideas that invite the neuroethologist’s scrutiny—processes that enlarge sensory capacities, accelerate thinking, and specify actions that can help an organism or population cope with real, perceived, or anticipated changes in the physical or psychological environment.  Even dissonance can activate the mechanisms of stress and emotion which have amongst their consequences an enhanced intensity of perception, cognition, and expression (Greenberg et al, 2002).

Any of these processes—perception, cognition, or expression—can be the initial focus of the neuroethologist’s perspective on creativity and art.  How do specific kinds or configurations of stimuli affect the brain? What qualities of stimuli can evoke memory and energize cognitive processing?  How do stimuli, perceptions, memories, and cognition interact to cause a specific action or emotional response?   Among the several starting points for an inquiry, I will emphasize the basal ganglia of the forebrain as an important coordinating and integrative center for the motor and cognitive functions that converge in creativity and thus in art and play.  I will also propose that elements of the physiological stress response are critical to energizing the creative processes.

Semir Zeki, a cognitive neurologist at University College, London, views the function of art as an extension of the visual function of the brain.  His concern is with the perceptive aspects of art—specifically, a “search for constancies with the aim of obtaining knowledge about the world” (1999a, p.79).  Taking the biologist’s approach, he has been able to obtain important information about the manner in which the brain extracts information from visual stimuli.  In this he claims that the artists themselves are also “studying the brain [but] with techniques that are unique to them . . . “ (1999b, p. 10).

In Brain and the Creative Act (1999), Karl Pribram presents his view that the hippocampal system, critical to memory and learning, may also play a role in creativity.  In particular, it appears to be more important to the process Arthur Koestler famously termed “bisociation” (1964).  Koestler coined this term to distinguish between routine thinking on a single plane, and creative thinking, which in his view always involves more than one plane. Pribram term describes this phenomenon as “recombinant processing of experience.”  Experience involves memory, although one may not necessarily be conscious of certain kinds of memories.  In Pribram’s book, Brain and Perception, (1991), Pribram develops the neurobiological underpinnings of his ideas on creativity including the fact that it often appears to depend on unique stimuli, or common stimuli uniquely construed, as a catalyst. Pribram pointed out that familiar stimuli can be perceived as novel (with an attending change in their salience) due to internally generated change such as a change in motivation.  When the ensemble of internal and external contexts confront little more than recurrent regularities, the system is relatively stable, but when stability is reduced, Pribram tells us, there is fertile ground for creative innovation.  When the “comprehensive contexts that map individual strategies become perturbed,” hippocampal activity is desynchronized, indicating that “the critical vectors that specify each context are no longer aligned within the map but come to point along many independent directions . . . , “ leading to the possible discovery of new paths (Pribram 1991, and see his Appendix F).

THE BASAL GANGLIA: FUNCTIONS OF THE CORPUS STRIATUM

The corpus striatum of the basal forebrain is also identified by clinicians as the basal ganglia.  This constellation of structures is represented in Paul D. MacLean’s famous triune brain model as the “R (for “reptilian”) complex,” sometimes playfully nicknamed, “The Beast in the Brain.”  MacLean has analyzed the anatomy and functions of this area in detail in his magisterial The Triune Brain in Evolution (1990), where he also points out the naive but persistent view of basal ganglia as principally regulating motor functions and relatively primitive stereotyped behavioral patterns.  The view that MacLean foresaw and now emerging is that the basal ganglia are also involved in many cognitive functions. 

In many respects, the study of basal ganglia functions presents an exemplar of the Alogic of the lamppost.”  Employing this seductive mode of reasoning, traditionally treated by analogy with looking for lost keys in a dark parking lot where we can search only under the illumination of a solitary lamppost, we tend to forget that the keys may yet be discovered someplace in the darkness.  Our illumination until quite recently has been the more easily discerned clinical evidence of motor dysfunction as a consequence of striatal damage.  The dramatic motor problems (e.g., Parkinson’s Disease) attributable to impaired basal ganglia have dominated perceptions of its function for generations, but among the symptoms of the “Shaking Palsy” described early in 1817 by James Parkinson was an impairment of intellectual and cognitive processes (“bradyphrenia”) with an associated depression sometimes preceding the more overt neurological symptoms.  Autonomic dysfunctions are also present and physical or psychological stress can alter the clinical profile in one of two ways:  “freezing,” an exacerbation or precipitation of neurological deficits, or “paradoxical kinesia,” a transient remission of bradykinesia when confronted with a life‑threatening emergency (Brown & Marsden 1998).

The presumed dependence on dopaminergic function believed to be at the heart of certain movement disorders was however, being shadowed by other interesting observations.   Synapses utilizing dopamine (DA) as a neurotransmitter have been of interest since the 1960s when some anti‑schizophrenic drugs were found to have their principal effect by binding to and blocking D2 receptors.  This complemented the finding that DA agonists (such as amphetamine) cause schizophrenic‑like behavior. Dopamine, then, is implicated in cognitive as well as motor functions of the basal ganglia (see Roffler and Graybiel, 1984).  Even basic personality traits are associated with dopamine.  More recently, slight variations (attributable to genetic polymorphisms) in specific dopamine receptors were found to be associated with specific personality types such as “novelty seekers” or “reward-dependent” (Ebstein et al. 1996, 1997).

The basal ganglia can in fact, constitute a series of  interfaces between cognitive, affective, and motivational functions that may be relevant to our consideration of neural influences on creativity (Greenberg et al., 2002).  Among the functions identified with the basal ganglia are acquisition, retention, and expression of cognitive patterns (Graybiel,1997), activation related to expectancies (Schultz,1998; Cotterill, 2001), selective attention (Parent, 1986, p.247), as well as A… focused and sustained attention in concert with flexibility of thought … planning and regulation of adaptive and goal directed behavior … [utilizing] working memory …” (Peigneux et al., 2000).

Novelty is important.   Novelty is a critical element of creativity.  Of course all growth and change deals with novelty and what is novel to a student may be routine to a teacher.  All forms of memory are demanding processes, but only novel stimuli or configurations need mobilize the brain’s machinery.  The organism thus possesses a fundamental need to identify novelty and its possible salience.  And many organisms, particularly at appropriate developmental stages, are eager seekers after novelty.  In a stable environment, in time the cost of seeking novelty may exceed its benefit, but there are always other environments.  The intrinsically motivating quality of novelty can evoke the sense of pleasure centered in the basal ganglia—one of the brain’s most powerful mechanisms for energizing the process that can lead to consolidation of memory.  The caudate nucleus has recently been found to integrate visual inputs with motivational values in the control of specific motor patterns (Kawagoe et al, 1998).   With respect to the importance of novelty, the activity of the neurones in the basal ganglia are controlled by the neurotransmitter dopamine produced lower in the neural axis in the substantia nigra and ventral tegmental area.  Although rewarding stimuli activate these structures, the activation is more intense when the reward is unexpected (Hollerman and Schultz, 1998).  The nucleus accumbens is a ventral striatal site regarded as essential to reward and thus learning (as well as addiction), but its activation by dopamine may depend more on novelty or the expectation or reward than on reward per se (Garris et al., 1999).  The path by which emotion (affect) enters the picture involves what is sometimes called the “extended amygdala,” a series of structures connecting the amygdaloid nuclei, long known to be critical to the expression of emotions, with the nucleus accumbens.  Its “downstream” connections then, affecting the hypothalamus and brainstem, constitutes what may be called an “emotional-motor” interface (Alheid and Heimer 1996).

Input, integration, and output.  All behavior is controlled by various proportions of internal and external stimuli.  When external information is compared to or integrated with internal information, an appropriate response can be selected.  Many responses are reflexive, highly programmed, or especially easily acquired, possibly in the context of play and other forms of practice that integrates the input (sensory), integrative, and motor functions of the nervous system into automatized sequences.   The frontal cortex complements and extends this process by the conscious use of mental models to help us pick an appropriate action—it is our organ of planning and prediction, of imagination.

Behavior is the outcome of the interaction of external and internal factors.  The readiness to perform any specific response is profoundly affected by its real (or perceived) biological relevance.  Specific responses are provided with more or less highly automatized programs of control depending upon the relative urgency of the biological function they serve–they can be conceived as more or less motivated.  Thus, the most fundamental biological needs (such as maintaining the stability of the physiological environment—homeostasis) or self-preservation, (Maslow 1954) has highly automatized programs of control.  Motivation therefore reflects real or perceived biological urgency and is profoundly affected by the real or perceived environment.

Familiarity and strangeness.  Relative novelty of a stimulus is a dimension of experience that can profoundly affect an organism’s relation to its environment.  It cannot be simple because organisms have a need for stimulation in order to maintain tone that will maintain readiness for future likely responses.  If stimulation is sufficiently deficient, organisms are stressed in ways that evoke compensating mechanisms, often resulting in anomalous and/or dysfunctional experiences ranging from pathological boredom through hallucination.   MacLean (1990) regards familiarity and strangeness as “indeterminate affects” (emotions) partly because their subjective agreeableness or disagreeableness is context-dependent.  He noted that these episodes of emotion affects may alternate during the aura preceding a psychomotor seizure, suggesting “a reciprocal innervation of affects that compares to the reciprocal innervation of muscles” (p. 450).

What sorts of effects might novelty have on the brain? For example, what brain areas might be affected as novel versus familiar pictures are being studied.  Tulving (et al., 1996) visualized brains in volunteers as they were doing just that, and he was able to determine that “Familiarity activations, signalling aspects of retrieval, were observed in the left and right frontal areas, and posterior regions bilaterally.”

Cotterill (2001) identified processes described by Carpenter that may articulate with the process of creativity:  the “race-to-threshold” mechanism (see Carpenter and Williams, 1995) and the randomization of behavior (Carpenter 1999).  The creative dimension emerges from unexpected correlations which may constitute novelty.  When these correlations are “captured” by areas such as the ventral striatum which will be activated when stimuli appear in an unanticipated context, the potential for creative associations will be enhanced by their feedback  serving a wider spread than feed-forward counterparts (Zeki and Shipp, 1988).

If this scenario proves to be reliable, it would indicate that the neural connectedness between areas is a vital ingredient in creativity.  But while rich connections might be something that one is born with, experience, particularly during an infant’s first two years, can contribute significantly to further enrichment.   The study of how connections between neurons are created and dissolved and how their fields of influence expand and contract has an enticing parallelism with ideas about how creativity itself works.  Indeed, the  connectionist model of neural function has been a powerful source of insight and provocative hypotheses for neurobehavioral scientists to examine (see for example, Boden 1990).  The  connectionist model involves both ephemeral and permanent changes in the nervous system from the synaptic level through the interactions of specific, anatomically or cytochemically definable neural structures.  The foundations of the approach are relatively recent, having found much recent support in the views of Gerald Edelman, who deals in detail with the dynamic nature of brain function in his book, Neural Darwinism (1987).

HOW STRESS AFFECTS CREATIVITY.

Stressors are stimuli that organisms perceive as challenges to their ability to meet their needs.  They typically evoke a stereotyped ensemble of physiological coping responses which can vary depending on the perceived urgency of the need.  In most vertebrates, depending on the intensity and timing of the stressor, the response is constrained by a threshold for detection of the stimulus, by attention based on apparent relevance, and by capacity to respond.  While related, each of these can vary independently.  Unfortunately, the popular view of stress is dominated by a model deeply informed by medical concerns about its harmful effects when experienced in excess.  Our modern view of stress and its potential for harm was forged by the incredibly productive Hans Selye.  Selye identified a “General Adaptation Syndrome” in which the initial response to an emergency (the sympathetic nervous system harnessed to the adrenal medulla which produced epinephrine and norepinephrine) was supplanted by a response in which the hypothalamic part of the brain initiated responses involving the anterior pituitary gland (producing ACTH) and the adrenal cortex (producing corticosteroid hormones).  These responses were mobilized when the organism was confronted with an acute repeated or sustained stressor (Selye 1936, 1956).  The process reallocates resources to cope, but sustained stress can lead to potentially deadly Adiseases of adaptation.”  Years later Seymour Levine (1971) reported that effective behavior depend upon some optimal level of stress,  and now we know that it is involved at many levels, all unified by the organism’s desire to cope.  For example, as Goldstein (1990) observed, dissonances that might occur when expectations are not met or when there is a mismatch between internal understanding and external experience, can evoke the neural pathways and physiological machinery of the stress response.  The behavioral patterns evoked by the stress response are typically very effective in coping with the stressor, but they can also overcompensate or exacerbate behavioral dysfunctions (Antelman and Caggiula 1980).

Stress as a basis for adaptive behavior.  Many behavioral patterns originated as responses to acute stressors but have subsequently been transformed and incorporated into the behavioral repertoire when it is adaptive to do so.  The neurophysiological input, integration, and action paths of the stress response may be utilized to cope with certain predictable events in an organism’s life history.  For example, when appropriately stimulated, the stress axis can evoke changes in activity levels or motivation to eat in preparation for seasonal life style changes such as migration or hibernation (Lee & McDonald, 1985; Silverin 1997, Wingfield, et al., 1997, Ramenofsky, 1990; other references in Greenberg et al.,  2002).   More famously, many signals exchanged by social species can be seen to have built upon functions originally designed to conserve metabolic resources when stressed, such as changing circulation of blood or thermoregulation.  Desmond Morris’s (1956) observation that many social signals in birds utilize feathers, the primary function of which is thermoregulation, led to his review of the concept of ritualization—the evolutionary changes in reflexes or fragments of a motor pattern that lead to a social signal.  Autonomic reflexes are key element of the stress response,  and the neural and endocrine support for thermoregulatory feather fluffing that Morris observed  is much like that utilized in courtship feather fluffing or even the male peacock’s spectacular tail display.  Relevant for our interests, another consequence of stress involves neural changes that can enhance cognition, evoke affect, and energize motivation.

Two related dimensions affect the profile of endocrine response and neural activity: the positive or negative affect associated with the stressor and the sense of controllability over then stressor.  The emotions identified with one’s experience of stress can be positive or negative, but all involve the activation of the same key neural and neuroendocrine pathways and always demand resources.  Thus, the physiological demands of positive stress (Selye’s “eustress”) can contribute as much as negative stress to the exhaustion of resources.  There is however, an important element of the perception of positive versus negative stress that cannot be overestimated.  When considering psychological variables, it is the perception of stress that is relevant.  In the absence of trauma or tissue damage, the body mobilizes resources as though in anticipation of an impaired ability to meet its biological needs.  But the pattern of stress responses depends to a large measure on the perception of the utility of a specific tactical response—that is (for example) the decision to attack or flee depends on an estimate of the prospects for success.  Costs and benefits of specific responses are assessed at several potential levels of response (including cognition) and the most efficient of alternative behavioral patterns are energized.  In other words, alternative strategies are apparently evoked by this perception of controllability (see for example, Cabib & Puglisi‑Allegra 1996, Huether 1996).   When there is a perception of lack of control or a sense of helplessness, organisms tend to intensify their conservation of resources (see Seligman 1975).  This is a significant contribution to Adiseases of adaptation” involving depressed behavior as well as impaired functions of digestive, reproductive, or immune systems.

The intensity of the stress response is important to the evocation of specific compensating mechanisms, including behavior.  A well-known example of this is the tendency of mild stress to energize activity and intense stress to paralyze it (Leshner, 1978).  Another apparent shift in response programs apparently dependent upon the intensity of the stress response is manifest in the suppression of prefrontal cortical (cognitive, planning) activity. The frontal cortex evolved in part to liberate the animal from proximate environmental control by the environment.  This adaptive innovation is frivolous next to basic biological survival needs and stress appears to take the prefrontal cortex >off-line’ to allow more habitual responses mediated by posterior cortical and subcortical structures to regulate behavior (Arnsten, 1997).  Another comparable pattern may be the impairment of hippocampal activity with commensurate facilitation of the amygdala that suggests, as LeDoux (1996) put it,  “the possibility that stress shifts us into a mode of operation in which we react to danger rather than just think about it” (p. 247).   The threshold for switching between more or less executive and automatic control of behavior likely changes with development.  For example, children may be particularly sensitive to stressful or traumatic experiences (Mayes, 2000), which may cause enduring changes in the brain.

Stress and cognition.  With respect to its influence on cognition, deKloet (et al. 1999) observed that while cell damage in specific parts of the brain can be caused by extreme stress (for example, post-traumatic stress disorder) the hormones responsible more normally protect the brain and are necessary for cognition.  Part of this apparent paradox is resolved by the fact that there are two kinds of adrenal cortical steroid hormones which affect the brain in different ways.  While activation of corticosteroid-receptors in the brain usually favor adaptive coping behavior involving changes in attention and selection of appropriate responses, if the two corticosteroid-receptor types are imbalanced for a prolonged period of time, maladaptive responses can be evoked.  Further, the stage of ongoing information processing (acquisition, consolidation, retention) affects the manner in which the brain responds to the hormones.

CONCLUSIONS

Defining creativity in biological terms broadens the scholarly and applied contexts in which it can be investigated and in which insights gained might be applied.  By reconfiguring our perception of creativity in terms of the ethologist’s collaborative developmental, ecological, evolutionary, end physiological approaches, our understanding of the biology of stress and the functional neurophysiology of the basal ganglia can be put in the service of understanding the causes and consequences of creative behavior and its key beneficiaries—art and science, and its key corollaries—play and learning.

Neurophysiology helps us appreciate the extent to which creativity involves the confluence of cognition, affect, and motivation in the basal ganglia of the forebrain.  Stress biology helps us understand the importance of dissonance and the ways in which the creative process can be energized or stultified by the autonomic neural and endocrine systems.  And ethology helps us view creativity as an evolutionary extension of the more mundane processes involving the accommodation and assimilation of novel experiences as we learn.  Informed by connectionist ideas of cognitive neuroscience and inspired by the well-known evolutionary process of ritualization, we can truly view creativity as “the peacock’s tail of development,” the discovery of connections, both novel and adaptive, between elements of our world.

REFERENCES

Alexander, Richard. (1989).  The evolution of the human psyche.  In P. Mellars and C. Stringer, (Eds.) The human revolution: Behavioral and biological perspectives on the origins of modern humans, pp. 455-513. Princeton, NJ:  University Press.

Alheid, George F. and Lennart Heimer.  (1996).  Theories of basal forebrain organization and the Aemotional motor system.”  Progress in. Brain Research 107, pp. 461-484.

Andre Breton (1955). Les manifestes du surrealisme. Cited by Marcuse 1955.

Antelman, S. M. and Caggiula, C. A. (1980).  Stress induced behavior: chemotherapy without drugs.  In J. M. Davidson and R. J. Davidson (Eds.).  The Psychobiology of Consciousness, pp. 65-104. New York: Plenum Press.

Aristotle.  (1962).  The politics. (E. Barker, Trans.).  Oxford University Press

Arnsten, A.F.  (1997).  Catecholamine regulation of the prefrontal cortex. J. Psychopharmacology, 11(2), pp.151-162.

Bardo, M.T., Donohew, R.L., Harrington, N.G. (1996).   Psychobiology of novelty seeking and drug seeking behavior. Behavioral Brain Research  77 (1-2), pp.23-43.

Berns, G.S., McClure, S.M., Pagnoni, G., Montague, P.R. (2001). Predictability modulates human brain response to reward.   J Neuroscience, 21(8), pp. 2793-2798.

Boden, Margaret.  (1990).  The creative mind.  New York:  Basic Books.

Bowers, W. J., Zacharko, R.M. and Anisman, H.  (1987).  Evaluation of stressor effects on intracranial self-stimulation from the nucleus accumbens and the substantia nigra in a current intensity paradigm. Behav Brain Res., 23, pp. 85-93.

Breuer, J. and Freud, S. (1937/1957). Studies on hysteria [Translated from the German and edited by James Strachey, in collaboration with Anna Freud, assisted by Alix Strachey and Alan Tyson] Basic Books, N.Y.

Brown, P. and Marsden, C.D. (1998).  What do the basal ganglia do?  The Lancet, 351, pp. 1801-1804.

Burghardt, G.M. (2001). Play: Attributes and Neural Substrates. Cambridge MA: MIT Press.

Burghardt, G.M. (1999).  Conceptions of play and the evolution of animal minds.  Evolution and Cognition.  5(2), pp.115-123.

Bussey, T.  (1999).   Novelty in the brain.  Trends in Cognitive Sciences. 3(4), p.126.

Cabib, S. and Puglisi‑Allegra, S. (1996). Stress, depression and the mesolimbic dopamine system. Psychopharmacology (Berl), 128 (4), pp. 331‑342.

Campbell, J. (1968).  The masks of God: Creative mythology.  New York: The Viking Press.

Cardinal, R.N., Pennicott, D.R., Sugathapala, C.L., Robbins, T.W., Everitt, B.J. (2001).  Impulsive choice induced in rats by lesions of the nucleus accumbens core.  Science 2001 May 24 [epub ahead of print in Science Express Reports, May 24, 2001. www.scienceexpress.org]

Carpenter, R.H.S. (1999).  A neural mechanism that randomizes behavior. J. Consciousness Studies, 6, pp.13-22.

Carpenter, R.H.S. and Williams, M.L.L. (1995).   Neural computation of log likelihood in the control of saccadic eye movements. Nature, 377, pp. 59-62.

Chapman, L.F., Walter, R.D., Markham, C.H., Rand, R.W. and Crandall, P.H. (1967).  Memory changes induced by stimulation of hippocampus or amygdala in epilepsy patients with implanted electrodes.  Trans. Amer. Neurol. Assoc.  92, pp. 50-56.

Coomaraswamy, A.K.  (1935/1956) Christian and oriental philosophy of art.  New York: Dover Publications.

Cotterill, R.M.J. (2001). Cooperation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: possible implications for cognition, consciousness, intelligence and creativity.   Progress in Neurobiology, 64, pp.1-33.

Crawford, C. (1998).  Environments and adaptations: Then and now.  In C. Crawford and D.L. Krebs (Eds.), Handbook of Evolutionary Psychology. pp. 275-302. Mahwah, NJ: Erlbaum.   

de Kloet, E.R., Oitzl, M.S.  and Joëls, M. (1999). Stress and cognition: are corticosteroids good or bad guys? Trends in Neurosciences  22 (10) pp. 422-426.

Dellu, F., Piazza, P.V., Mayo, W., Le Moal, M., Simon, H. (1996) Novelty-seeking in rats–biobehavioral characteristics and possible  relationship with the sensation-seeking trait in man. Neuropsychobiology 34 (3), pp.136-145.

Dewey, J. (1934).  Art as experience, pp.277-278. London: Geo Allen & Unwin.

Dissanayake, E. (1992). Homo Aestheticus: Where art comes from and why. New York: The Free New York: Press/Macmillan.

Ebstein, R.P., Segman, R., Benjamin, J., Osher, Y., Nemanov, L., Belmaker, R.H.  (1997).   5‑HT2C (HTR2C) serotonin receptor gene polymorphism associated with the human personality trait of reward dependence: interaction with dopamine D4 receptor (D4DR) and dopamine D3 receptor (D3DR) polymorphisms.  American  J Medical Genetetics,   74(1), pp.65‑72.

Ebstein, R.P., Novick, O., Umansky, R., Priel, B., Osher, Y., Blaine, D., Bennett, E.R., Nemanov, L., Katz, M., Belmaker, R.H.   (1996).  Dopamine D4 receptor (D4DR) exon III  polymorphism associated with the human personality trait of Novelty Seeking.  Nature Genetics 12 (1), pp.78‑80

Edelman, G.M.  (1987).  Neural Darwinism: The theory of neuronal group selection. New York: Basic Books.

Fagen, R.  (1981).  Animal play behavior.  New York: Oxford University Press.

Furlow, B. (2001).  Play’s the thing.  New Scientist, June 9: http://www.newscientist.com/features/features.jsp?id’ns229412 .

Garris, P. A., Kilpatrick, M. Bunin, M.A., Michael, D., Walker, Q.D. and Wrightman, R.M.  (1999).   Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature, 398, pp. 67-69.

Goldstein, D.S.  (1990).  Neurotransmitters and stress.  Biofeedback and self‑regulation, 15 (3), pp. 243‑272.

Graybiel, A. M.   (1997).  The basal ganglia and cognitive pattern generators. Schizophr Bulletin, 23 (3), pp. 459-69.

Greenberg, N. (1998).  “The evolutionary physiology of creativity.”  Human Behavior and Evolution Society, Tenth Annual Meeting, University of California – Davis, July 12-13, 1998.  (Lecture)

Greenberg, Neil. (2002) Adaptive Functions of the Corpus Striatum: The Past and Future of the R-Complex in The Neuroethology of Paul MacLean: Frontiers and Convergences. ed. G. Cory and R. Gardner Praeger, London, 45-81.

Greenberg, N., Carr, J.A., Summers, C.H. (2002).  Ethological Causes and Consequences of the Stress Response. J Integrative and Comparative Biology. 42(3):508-516. https://www.researchgate.net/publication/51253242

Hamilton, W.D.  (1964).  The genetical evolution of social behaviour I, II. J Theoretical Biology 7, pp. 1-52.

Herve, D., Blanc, G., Glowinski, J., Tassin J.P. (1982.)  Reduction of dopamine utilization in the prefrontal cortex but not in the nucleus accumbens after selective destruction of noradrenergic fibers innervating the ventral tegmental area in the rat.  Brain Research  237, pp. 510-516. 

Hockett, C.F. and Ascher, R. (1964). The human revolution, Current Anthropology, 5 (3), pp.135‑168.

Huether G. (1996.) The central adaptation syndrome: psychosocial stress as a trigger for adaptive modifications of brain structure and brain function.  Progress in Neurobiology,  48 (6), pp. 569-612.

Hollerman, J.R. and Schultz, W. (1998). Dopamine neurons report an error in the temporal prediction of reward during learning.  Nature Neuroscience 1(4), pp. 304-309.

Hutson, J. H.  (1981).  Creativity: A continuing inventory of knowledge.  Library of Congress, Washington, DC.

Huzinga, J. (1949).   Homo ludens: A study of the play‑element in culture. [Tr. by R. F. C. Hull] London: Routledge & Kegan Paul.

Kawagoe, R., Takakawa, Y., Hikosaka, O. (1998).  Expectation of reward modulates cognitive signals in the basal ganglia.  Nature Neuroscience, 1 (5), pp. 411-416.

Kihlstrom, J. F. (1987). The cognitive unconscious. Science 237, pp.1445‑1452. 

Koestler, A.  (1964). The act of creation. New York: Macmillan.

Klopfer, P.H. (1970). Sensory physiology and esthetics.  American Scientist, 58, pp. 399-403.

Knight R.T., Nakada, T. (1998).  Cortico-limbic circuits and novelty: a review of EEG and blood flow data. Rev Neurosci, 9, pp. 1, 57-70.

Krentz, A. A.  (1998). Play and education in Plato’s Republic. Paper presented at the Twentieth World Congress of Philosophy, Boston, Massachusetts, August 10-15, 1998.  Accessible at the Paideia Project On-Line, Boston University (downloaded June, 2001)  (http://www.bu.edu/wcp/Papers/Educ/EducKren.htm).

 Kris, E. (1952).  Psychoanalytic explorations in art. New York: International Universities Press.

Kroeber, A.L. (1948).  Anthropology, N.Y.

LeDoux, J. (1996). The emotional brain. New York: Simon & Schuster.

Lee, A.J.K. and McDonald, I.R. (1985). Stress and population regulation in small mammals. In J.R. Clarke (Ed.) Oxford Reviews of Reproductive Biology Oxford: Clarendon Press,  pp. 261-304. 

Levine, S.  (1971).  Stress and behavior. Scientific American, 224 (1), pp. 26-31.

Leshner, A. (1978).  An introduction to behavioral endocrinology.  New York: Oxford University Press.

Lorenz, K. Z.  (1981).  The foundations of ethology. New York: Simon and Schuster.

MacLean, P.D. (1990). The triune brain in evolution. New York: Plenum Press.               

Marcuse, H. (1955).  Eros and civilization: A philosophical investigation into Freud.  Boston: Beacon Press.

Maslow, A. (1954). Motivation and personality. New York: Harper.

Martindale, C. (1999). Biological bases of creativity. In R. Sternberg (Ed.) Handbook of Creativity.   Cambridge University Press, pp. 137-152.

Mayes LC. (2000). A developmental perspective on the regulation of arousal states. Semin Perinatol, 24 (4), pp. 267-279.

Merriam-Webster’s Dictionary [on-line] available:  http://www.m‑w.com/cgi‑bin/netdict

Mook, D.G. (1996). Motivation: The organization of action. New York: W.W. Norton.

Morris, D. (1962). The biology of art. Knopf, N.Y.

Morris, D. (1956). The feather postures of birds and the problem of the  origin of social signals.          Behavior, 9, pp. 75‑113. 

Nesse, N.C. and Berridge, K.C. (1997). Psychoactive drug use in evolutionary perspective.        Science. 278, pp. 63 ‑66.

Novitz, D. (1987). Knowledge, fiction and imagination. Philadelphia: Temple University Press.

Paradiso S., Johnson, D.L., Andreasen, N.C., O’Leary, D.S., Watkins, G.L., Ponto, L.L.B,  Hichwa, R.D. (1999). Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. American J. Psychiatry, 156 (10), pp.1618-1629.

Parent, A, (1986).  Comparative neurobiology of the basal ganglia. Wiley, New York.

Parker A., Wilding, E. and Akerman, C. (1998). The von Restorff effect in visual object recognition memory in humans and monkeys: the role of frontal/perirhinal interaction.  J. Cognitive Neuroscience,10, pp.691‑703.

Peigneux P, Maquet, P., Meulemans, T., Destrebecqz, A., Laureys, S., Degueldre, C., Delfiore, G., Aerts, J., Luxen, A., Franck, G., Van der Linden, M., Cleeremans, A. (2000).  Striatum forever, despite sequence learning variability: a random effect analysis of PET data.  Human Brain Mapping. 10 (4), pp. 179-194.

Poincaré, H. (1913). The foundations of science. Lancaster, PA: Science Press.

Pribram, K.H. and McGuinness, D. (1975). Arousal, activation and effort in the control of attention. Psychological Reviews, 82 (2), pp.116-149.

Pribram, K.H. (1999). Brain and the creative act. 1999. Encyclopedia of Creativity, New York: Academic Press, pp. 213-217.

Pribram, K. (1998). On brain and value: Utility, preference, play and creativity. In: Brain and values: Is a biological science of values possible?  Pribram, Karl H. et al., (Eds.). Mahwah, NJ: Lawrence Erlbaum, pp. 43-54.

Pribram, K. (1991). Brain and perception. Hillsdale, NJ: Lawrence Erlbaum. 

Ramachandran, V.S. (1998). The neurology and evolution of humor, laughter, and smiling: the false alarm theory. Med Hypotheses, 51 (4), pp. 351‑354.

Ramachandran, V.S. (2000). Concerning “the science of art:” Response from V.S. Ramachandran. Journal of Consciousness Studies, 7 (8-9), pp. 17-20.

Ramachandran, V.S. Hirstein, W. (1999). The Science of art: A neurological theory of aesthetic experience. Journal of consciousness studies, 6 (6-7), pp.15-51.

Random House Dictionary of the English Language. (1987). Second edition, Unabridged. Random House, New York

Raminofsky, M. (1990). Fat storage and fat metabolism in relation to migration. In: E. Gwinner (Ed.), Bird Migration: Physiology and Ecophysiology, pp. 214-231. Berlin, Springer-Verlag.

Rizzolatti, G. and Arbib, M. (1998). Language within our grasp. Trends in Neurosciences, 21, pp. 188- 194.

Roffler-Tarlov S., Graybiel, A.M. (1984). Weaver mutation has differential effects on the dopamine-containing innervation of the limbic and nonlimbic striatum. Nature, 307, pp.62-66.

Rozin, P. (1976). The evolution of intelligence and access to the cognitive unconscious.  Progress in Psychobiology and Physiological Psychology, 6, pp. 245‑ 280.

Schultz, W. (1998). Predictive reward signal of dopamine neurons. J Neurophysiology,   80 (1), pp. 1-27.

Seligman, M. (1975). Helplessness. San Francisco: Freeman & Co.

Seligman, M, Rosellini, R. and Kozak, M. (1975). Learned helplessness in the rat. J. Compar. Physiol. Psychology, 88, pp. 542-547.

Selye, H. (1936). A syndrome produced by diverse nocuous agents. Nature, 138, p. 32. Cited by Johnson et al. 1992.

Selye, H. (1956). The stress of life. New York: McGraw Hill. 

Silverin, B. (1997). The stress response and autumn dispersal behavior in willow tits. Animal Behaviour, 53, pp. 541-549.

Taylor, J.A. (1999). Koans of silence: The teaching not taught. Parabola, 24 (2), pp. 6-11.