Introduction

Steroid hormones produced in the gonads are a prerequisite for mating behavior in the male Syrian hamster, as in most male mammals. While a substantial body of early research was directed toward defining the hormonal requirements (both quantity and identity) for this behavior, more recent studies have focused on hormone metabolism, receptor distribution, and mechanisms of steroid action in the central nervous system (CNS). This chapter explores the transduction of hormonal signals by steroid receptor–containing neurons to facilitate sexual behavior in the male hamster.

Hormonal requirements for copulation

Copulation in the male Syrian hamster

The sequence of copulation in the male Syrian hamster has been reviewed previously (Siegel 1985; Sachs and Meisel 1988). However, a brief description of the behaviors expressed during mating would be helpful for understanding the critical role that hormones play in maintaining this activity. Figure 1.1 illustrates sexual behavior over a 10-minute period in a sexually experienced male. Initial contact with a receptive female is characterized by investigation of the female's head and flank, followed by extensive sniffing and licking of the anogenital region. Through this activity, the male receives chemosensory stimulation via the vomeronasal organ and olfactory mucosa. The ability to perceive chemosensory signals and the integrity of the neural pathways that transmit chemosensory stimuli are essential for copulation, because disruption of chemosensory cues immediately and permanently abolishes mating (reviewed by Sachs and Meisel 1988). In a sexually experienced male, anogenital investigation of the female is followed shortly by a series of mounts and intromissions, interspersed with brief (1- to 2-second) grooming of the penis and perineum.

Introduction

During development and adulthood, the central nervous system (CNS) undergoes structural and neurochemical changes under the influence of endogenous stimuli. Among these stimuli are sex steroid hormones synthesized by the gonads, adrenal cortex, and CNS cells themselves (see Chapter 12 by Robel and Baulieu and Chapter 13 by Schlinger and Arnold, this volume). Sex steroid–sensitive neurons provide the anatomical substrate at which sex steroid hormones affect the structure and function of the CNS. Generally, these cells respond to the action of sex steroid hormones either directly, through hormone–receptor interaction, or indirectly, through trans-synaptic activation of membrane receptors and subsequently second messengers or immediate early genes.

In vertebrate species, most sex steroid–sensitive cells are part of the sexually differentiated limbic–hypothalamic circuit, which, within a more expansive neural network, controls reproductive events. To understand the functioning of the limbic–hypothalamic circuit, we must determine how sex steroids specify chemical connections within this circuit and how steroid hormone–induced changes in these connections are related to the display of sexual behavior. The phylogenetically conserved limbic–hypothalamic circuit consists of the posterior dorsal medial amygdala (MeA), encapsulated bed nucleus of the stria terminalis (BNST), medial preoptic nucleus (MPN), and ventromedial nucleus of the hypothalamus (VMH) (reviewed by Micevych and Ulibarri 1992). This circuit integrates a variety of neuronal inputs carrying somatic, olfactory, and hormonal information and sends projections to effector circuits to initiate neuroendocrine events (gonadotropin release) and sexual behavior (mounting or lordosis, reviewed by Pfaff and Schwartz-Giblin 1988).

Introduction

Circulating gonadal and adrenal steroid hormones readily cross the blood–brain barrier and affect neural circuits that subserve various aspects of brain function and behavior. When investigating the interactions between hormones and neurotransmitter systems, it is particularly important to study a model system where there is a behavioral endpoint for which the neural control sites are discrete and accessible. Mating behavior in the female rat provides such a system (Pfaff 1980). The ovarian steroid hormones estradiol (E) and progesterone (P) synchronize the occurrence of mating and ovulation, and thereby increase the likelihood of reproductive success. Our goal is to take advantage of this useful model system in order to elucidate the mechanisms of steroid hormone action on neuronal activity and connectivity. In addition to enhancing our knowledge of the specific events that control this biologically important behavior, such studies may have broader implications for the analysis of hormone–neurotransmitter interactions.

It is well known that ovariectomized (OVX) female rats display very little sexual behavior. Estradiol replacement reverses this condition, however, by sensitizing specific neural circuits to stimuli that elicit sexual behavior. Approximately 48 hours after E is administered, OVX female rats display sexual behavior when they encounter a male. Progesterone treatment, given after E and about 4 hours before behavioral testing, further enhances female sexual behavior (Boling and Blandau 1939). Treatment with P is ineffective unless the animals have been primed with E, in part because E induces expression of a subset of P receptors (MacLusky and McEwen 1978).

The presence of specific steroid receptors in neurons and evidence of steroid binding provide a basis for understanding the direct effects of steroids on neuronal function. Yet many key actions of gonadal steroids may be transmitted through multisynaptic pathways, in which only a subset of the participants are directly steroid-sensitive. The exploration of steroid actions on multisynaptic neuronal systems is nonetheless important but has been complicated by the lack of experimental techniques for monitoring activity changes across brain areas. In recent years, scientists have recognized that Fos, the protein product of the c-fos immediate early gene, is expressed in neurons that are stimulated. Immunocytochemical staining of Fos following specific stimuli has proved valuable for assessing neuronal activity (Morgan and Curran 1989; Sagar et al. 1988), and the results of studies using this approach will be presented here.

Specifically, the studies summarized in this chapter examined certain effects of gonadal steroids on neuronal activity as assessed by Fos staining. Two principal lines of investigation will be discussed. The first is the role of estrogen and progesterone in the luteinizing hormone–releasing hormone (LHRH) neuron activation that drives the preovulatory LH surge. The second is the role of progesterone in modifying neuronal activation by excitatory amino acids in brain systems other than the LHRH neurons. The latter studies point to the global effects that gonadal steroid hormones can have on neuronal function distinct from their actions on the regulation of reproductive function.

Substance P is the best-known member of the family of tachykinin (TAC) peptides. Its distribution in spinal ganglia and substantia gelatinosa of the dorsal horn initially suggested a role in the transmission of sensory information from the periphery to the central nervous system (Hokfelt et al. 1975). Subsequently, an extensive distribution in the limbic system and brain stem (Ljungdahl et al. 1978) implicated these peptides in integrative and other processes as well. Mammalian TAC peptides are derived from two separate genes, usually designated preprotachykinins A and B. Preprotachykinin A mRNA codes for substance P, neurokinin A (NKA), neuropeptide K (NPK), and neuropeptide γ (NKγ; Krause et al. 1990), and preprotachykinin B mRNA codes for neurokinin B (NKB). Thus, the rat central nervous system contains at least five TAC peptides (Arai and Emson, 1986; Takano et al. 1986; Takeda et al. 1990; Tatemoto et al. 1985). Although substance P has a well-established role in the regulation of luteinizing hormone–releasing hormone (LHRH) secretion and sexual behavior, reproductively relevant roles for other TAC peptides are only now being explored. Much of what we can infer about the functional roles of TAC peptides in the central nervous system is derived from immunohistochemical studies, but antibodies to substance P often cross-react with other TAC peptides. Therefore, we have used the term “TAC-immunoreactive” (TACir) to describe the labeling of cells using antibodies directed against these peptides.

Psychosis and psychoticism

In previous chapters we have seen that while psychopathology was clearly enmeshed with genius and creativity, the usual psychiatric concepts, e.g. psychosis, were clearly counter-indicated; psychosis (schizophrenia, manicdepressive disorder) was rarely found in geniuses, equally rarely, in creative writers, mathematicians, scientists, or architects, and in any case its diagnosis was so unrealiable, even in live patients studied intensively, that diagnosis on the basis of accounts written centuries ago would be pretty worthless. An even more serious objection would be that the orthodox psychiatric system of nosology is not in line with modern discoveries, and entails many serious defects. The major defect, which is absolutely fundamental, concerns the notion that psychiatric disorders differ qualitatively from normality, just as tuberculosis, or malaria, or mad cow's disease is differentiated qualitatively from healthy normality. Such a categorical differentiation was already criticized by Kretschmer (1936, 1948) and many others, and does not accord with reality (Claridge, 1985). This point will be discussed in more detail presently.

A very relevant weakness, often noted in psychiatric nosology, is the reliability of diagnoses; different psychiatrists very frequently apply different diagnostic labels to a given patient. It is frequently claimed that the arrival of DSM-III, the Diagnostic and Statistical Manual of Mental Diseases, published by the American Psychiatric Association, has overcome this difficulty, and that now all is plain sailing. A recent book by Kirk and Kutchins (1992) has shown clearly that these claims, often made by official sources, are quite unjustified; parturient montes nascetur ridiculus mus! (The mountains will be in labour, to produce a ridiculous little mouse! Horace.)

Creativity and psychoticism

In this chapter I will review the evidence that P is indeed associated with creativity, both conceived as a trait, and conceived of as achievement. This demonstration is central to the causal theory developed later in the chapter, trying to link creativity with biological mechanisms and the genetic basis of creativity with creative behaviour.

Any theory linking creativity and psychoticism must of course be validated by empirical research, along a number of different lines. One line of research has consisted of using psychosis-prone subjects as high psychoticism probands. As already mentioned, Heston (1966) studied offspring of schizophrenic mothers raised by foster-parents, and found that although about half showed psychosocial disability, the remaining half were notably successful adults, possessing artistic talents and demonstrating imaginative adaptations to life to a degree not found in the control group. Karlsson (1968, 1970) in Iceland found that among relatives of schizophrenics there was a high incidence of individuals of great creative achievement. McNeil (1971) studied the occurrence of mental illness in highly creative adopted children and their biological parents, discovering that the mental illness rates in the adoptees and in their biological parents were positively and significantly related to the creativity level of the adoptees.

We are now in a position to consider as a whole the model of genius and creativity that I have been at pains to construct from a variety of writers, psychologists and interested scientists. There are some novel aspects, but essentially the novelty lies in my attempt to make personality differences central to the argument. Previously personality traits were indeed studied, but were never given the central position I believe they deserve. The early indication that mental ability (IQ) is only loosely correlated with creativity has not usually been interpreted to suggest that creativity is not an ability, but a cognitive style closely related with psychoticism. It may be useful to set out the general theory in diagrammatic form (Fig. 8.1).

We start inevitably with heredity, embodied in a person's DNA (deoxyribonucleic acid). Practically all the variables we have found associated with creativity and genius have a genetic component. Creativity is associated physiologically with the hippocampal formation, and with the level of activity of dopamine and serotonin, the former heightening, the latter lowering creativity (regarded as a trait). It is suggested that their influence is directly on cognitive inhibition, i.e. cognitive factors like latent inhibition and/or negative priming, which reduce the tendency towards over-inclusiveness indicative of psychoticism, and, when lacking, in extreme form produce functional psychosis (schizophrenia; manic-depressive illness), and in lesser extent creativity. Thus, through the widening associative horizon associated with lack of latent inhibition and/or negative priming, psychoticism is closely linked with the trait of creativity.

Possessing this trait, however, does not guarantee creative achievement.

Stages of problem-solving

Two notions, ideas, concepts – call them what you like – have always been attached to the problem of creativity. Is has been widely surmised that the creative genius generates his major ideas by way of intuition, rather than rational thinking; reason can test and prove or disprove the insights achieved by intuition, but cannot produce them. Furthermore, the process by means of which intuition works is unconscious; the Unconscious, whether with or without a capital ‘U\ is the cradle of creativity. I will spell out some of the data on which this commonsense view rests (mainly anecdotal), and then go on to define the concepts experimentally.

Many famous scientists have identified stages of problem-solving; these nearly always include a central stage during which unconscious cerebration, mentation, or whatever predominates. Thus Helmholtz (1896) postulated an initial investigatory stage, during which he became saturated with the large body of relevant facts. This was followed by a stage of rest and recovery, during which he gave no conscious attention to the problem, and finally a stage of illumination, when he had sudden insight into the solution – the ‘aha!’ experience. Similarly descriptions are given by Dewey (1910), Rossman (1931), Osborn (1953), Johnson (1955), Cattell (1971), and Mansfield and Busse (1981). Wallas (1926) put various introspective accounts together in his frequently cited four-stage scheme: (1) Preparation; (2) Incubation; (3) Illumination; and (4) Verification. To these has recently been added a stage of Problem-finding, which precedes Wallas's stage one (Arlin, 1975; Bunge, 1967; Dillon, 1982; Chand and Runco, 1993).

Works of genius depend on the confluence of certain personality variables (intelligence, creativity, persistence, etc.) and certain social conditions; Newton, Mozart or Shakespeare would not have been able to show their true genius in a primitive culture. It is the purpose of this chapter to look at a number of social and other conditions, largely external to the individual, which facilitate or hinder the development of genius. It is not always easy to say whether these conditions have a direct causal influence on the production of works of genius, or the development of the genius himself. In epidemiology we distinguish between risk factors and causes. Risk factors are variables which are significantly correlated with specific diseases, but may not be causally related to them. Causes must be shown to be necessary and sufficient for the disease to develop. Koch's famous postulates were enunciated to give precision to this distinction, and make it clear just what was needed for a particular factor (such as the tubercle bacillus) to be regarded as a cause of tuberculosis, and not just as a risk factor.

In the scientific study of complex phenomena, this distinction is absolutely vital; we search for causal elements, but are only too often satisfied with what are mere risk factors. An example may make clear the distinction. In Denmark there has been observed over many years a correlation between the birth of a baby, and the presence of a stork's nest on the roof of the house where the baby was born.

Intelligence – a dispositional variable

Few writings on genius have neglected to give intelligence a very high place, and indeed it is difficult to think of leading philosophers, scientists, writers, statesmen and artists other than highly gifted intellectually. But the opposite does not follow; not all people who are highly gifted intellectually turn out to be geniuses – were it otherwise the world would be overrun with geniuses! Intelligence is a dispositional variable, i.e. it enables a person with that ability to solve certain problems, produce certain results, achieve certain aims, but it does not guarantee success. Very early in the history of psychometric testing, Alexander (1935) analysed the relation between ability and school grades and discovered an ‘X’ factor, which was found to run through all the school subjects but through none of the ability measures. Alexander stated: ‘We are suggesting that X must be interpreted as a character factor which exercises an important influence on success in all school subjects. If we were to attach a name to this factor, we should be inclined to call it persistence.’

The distinction between a dispositional variable and what we might call an achievement variable (e.g. school success, production of a work of genius) is absolutely vital in understanding psychological analyses of abilities and traits. The distinction currently made between trait and state, say of anxiety, embodies the distinction.

It is just over 50 years ago that I wrote my first article on the topic of intelligence (Eysenck, 1939). I was reviewing Thurstone's famous monograph (Thurstone, 1938) in which he criticized Spearman's (1927) theory of intelligence as a single entity or concept, spreading over all cognitive activities; he postulated instead a number of ‘primary abilities’, separate and uncorrelated. Reanalysing his very extensive data, I found evidence both for a general factor of intelligence, very much as postulated by Spearman, and also for a number of primaries, very much as postulated by Thurstone. Both Spearman (Spearman and Jones, 1950) and Thurstone (Thurstone and Thurstone, 1941) finally agreed that a hierarchical system of description of the cognitive space incorporating both a general factor of intelligence and various group factors or special talents, was most in line with the available facts, and there is now considerable consensus on some such system (Vernon, 1979; Eysenck, 1979; Brody, 1992; Carroll, 1993).

While quite happy with such an account at the descriptive level, I felt that if there was a strong genetic basis for IQ, as there undoubtedly is (Woodworth, 1941; Eysenck, 1979; Plomin, De Fries and McClearn, 1990), there must be some physiological or hormonal intermediaries between DNA and behaviour – it is impossible for DNA to influence behaviour directly.

Creativity: the beginnings of measurement

If intelligence is not sufficient to account for genius, we must look for other factors, and ‘creativity’ is perhaps more frequently suggested than most. Much work has been done to clarify the nature of this concept (Glover, Ronning and Reynolds, 1989), but much diversity of opinion remains. Taylor (1988) lists six types of definition, most of which are somewhat esoteric and unusual. For the purpose of orientation, we may perhaps say that creativity is a dispositional trait or ability which enables a person to put forward ideas, or execute and produce works of imagination, having an appearance of novelty, which are immediately or in due course accepted by experts and peers as genuine contributions having social value. In due course we shall flesh out this definition by reference to a large body of experimental and observational studies.

Any such experimental study must of course rely on tests or other measuring devices which can be shown to be valid measures of the concept. In order to do this, we must demonstrate (1) that such tests are not merely measures of g or general intelligence, and (2) that they possess some degree of unity or coherence (reliability). One would have thought that the first man to see the precise nature of the problem, find ways of solving it, and be responsible for suggesting how such tests could be constructed would find an honoured place in the history of creativity research.

Popular concepts of genius

There are many books on the topic of genius; since the days of Aristotle and Plato, philosophers, artists, teachers, scientists, psychiatrists and lately psychologists have combined to tell us what genius is, how it is produced, how it relates to madness, how it can be cultivated. These contributions consist of writings which rely on common-sense, historical anecdotes, and descriptive passages extolling the wonders of genius. Thus ‘genius’ is depicted as the possessor of a mystical gift that cannot be explained by the ordinary laws of human nature – a conclusion that would immediately make impossible the realization of the research project on which this book is based. It is possible to bring together popular notions of genius by citing a number of definitions. Some of these make genius seem remarkably commonplace. Thus for Buffon, genius was ‘but a great aptitude for patience’. Frederick the Great thought it was a ‘transcendent capacity for taking trouble’. Edison considered it ‘one per cent inspiration and ninety-nine per cent perspiration’, while Disraeli agreed with Buffon – ‘patience is a necessary ingredient of genius’. Thus we learn that genius means hard work, true but not very revealing. It may highlight the absurdity of modern educational methods which stress the alleged natural creativity of children, but refuse to impart the necessary knowledge without which creativity cannot function.

More interesting are quotations telling us about the creativity of genius.