How hormones affect behaviour

The effects of hormones on behaviour can be traced to four broad areas of influence:

the nervous system, sensory perception, effector systems and development. Techniques for studying them range from surgery (glandectomy) followed by hormone replacement to manipulation of circulating hormone concentrations (e.g. by injection, implants or cross-transfusion) and correlational studies (e.g. Figs 3.28 and 3.31). We discuss the effects of hormones on the development of behaviour in more detail in Chapter 6 (see 6.1.2); here we focus mainly on their role in mechanism.

3.3.1.1 Effects on the nervous system

Hormones affect many aspects of the nervous system, including anatomy, biochemistry and impulse transmission. In some cases, they may be responsible for basic structural and functional changes within the CNS. Reflex connections (3.1.3.2), for example, are accelerated by high levels of thyroxin, a hormone secreted by the thyroid gland.

Some sex differences in behaviour in rats are associated with sexual dimorphism in the anatomy of cells in the neuropile of the hypothalamus, a dimorphism that appears to be

mediated by neonatal levels of androgen (male steroid sex hormones secreted mainly by the testes) (Raisman & Field 1973). However, care is needed in interpreting the neuronal effects of hormones. For instance, progesterone and oestrogen (female steroid sex hormones) both enhance the responsiveness of neurons in the rat CNS to stimulation of the vaginal cervix. However, while the effect of progesterone is rapid and associated with a general increase in arousal of the animal, behavioural effects of oestrogen are usually not apparent for several days, implying longer-term changes in the state of neurons.

A given hormone can have very different effects on behaviour depending on the region of the CNS on which it acts. Nyby et al. (1992) looked at the effects of intracranial implants of testosterone (an androgen) in male house mice on various aspects of social and sexual behaviour, including ultrasonic vocalisations, urine marking, mounting and aggression. They implanted the hormone in one of four regions of the brain: the septum, the medial preoptic area, the anterior hypothalamus or the ventromedial hypothalamus.

Control animals were given subcutaneous implants of testosterone or empty implants in the appropriate region of the brain. The testosterone controls performed all the behaviours at the normal level for sexually responsive males, while the empty implant controls showed no response. When it came to the site-specific implants, however, Nyby et al. found a range of responses. Implants in the median preoptic area showed increased ultrasonic vocalisation, while those in other regions had little effect. Those in the medial preoptic or either hypothalamic regions resulted in more urine marking than empty implant controls, but less than testosterone controls. Mounting occurred in testosterone controls and males implanted in the median preoptic area, while aggression was rare in all males given brain implants. Together, the results thus suggest complex functional interactions between different areas of the brain containing testosterone receptors.

Rather than influencing behaviour directly through their effects on the nervous system, hormones may act as ‘primers’ facilitating the action of other hormones. In female hamsters (Mesocricetus auratus) primed with oestrogen, behaviour typical of oestrus can be induced by injecting small doses of progesterone into the brain ventricles.

If injected subcutaneously, or in the absence of oestrogen, such doses fail to induce the response. Similar priming effects, but in relation to electrical stimulation, have been 3.3 ⁿ Hormones and behaviour x ₁₄₅ Figure 3.28 Correlational evidence for a

relationship between circulating testos-terone concentration and aggression in male Egyptian spiny mice (Acomys cahirinus dimidiatus). The vertical axis scale is devia-tions from the sample mean. From Barnard et al. (2003).

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shown in rats. Electrodes implanted in a rat’s brain can be connected in such a way that the animal can simulate its own brain by pressing a pedal. Stimulation of some areas results in more frequent and persistent pedal-pushing than others. Olds (1961), how-ever, found that treating these areas with androgen could enhance the rat’s responses to a given level of stimulation.

In other cases, hormones may not so much exert a positive effect on the nervous system as remove inhibition. In neonatal guinea pigs (Cavia porcellus), the lordosis (female receptive) posture is an integral part of excretory behaviour. At first, excretion is stimulated by the mother, but, as the young mature, micturation and defaecation come under internal control mechanisms located in the spine. These spinal centres are subject to inhibitory control by the brain, and, as females become adult, inhibition of spinal control is relaxed by the secretion of ovarian hormones. Hormones may also establish inhibition. Oestrogen, for example, inhibits aggressive behaviour in female hamsters, while sexual receptivity in female grasshoppers is inhibited by hormones produced as a result of the spermatheca (female sperm storage organ) filling with sperm.

3.3.1.2 Effects on sensory perception

Many studies suggest that hormones affect an animal’s sensory capabilities. In doing so, they alter the animal’s perception of its environment and therefore the way it responds to particular stimuli. The seasonal migration of three-spined sticklebacks (Gasterosteus aculeatus) provides a good example. In spring, male sticklebacks migrate from the sea to their freshwater breeding grounds. In doing so, they move through water that gradually changes in salinity. To facilitate this transition, hormones secreted by the pituitary and thyroid glands, but particularly thyroxin, alter the fishes’ salinity preference from salt water to freshwater (Baggerman 1962).

In many female mammals, sensory perception is influenced by the oestrous cycle.

Female rats fluctuate in their ability to detect certain odours according to circulating levels of oestrogen and progesterone. Similarly, visual sensitivity in women varies with the stage of their menstrual cycle (and thus relative oestrogen and progesterone levels), being most acute around the time of ovulation, and least acute during menstruation, a difference that is abolished when taking oral contraceptives. In female rats, oestrogen also has the effect of extending the sensory field of the perineal nerve, which innervates the genital tract (Komisaruk et al. 1972). During oestrus, she is thus more responsive to the tactile stimulus of intromission, and orientates her body to facilitate penetration (lordosis; Fig. 3.29). In birds, oestrogen causes the formation of a ‘brood patch’.

Feathers are lost from part of the ventral body surface in females and the exposed skin becomes more heavily vascularised, thus increasing the sensitivity of the female to the nest cup and influencing her nest maintenance and incubatory behaviour.

Figure 3.29 Female rats take up the characteristic copulatory posture known as lordosis partly in response to the effects of oestrogen on the tactile sensitivity of the genital tract.

Sensory perception in males is also influenced by hormones. Sexually experienced male rats prefer the odour of urine produced by females in oestrus compared with dioestrus, but the preference disappears if males are castrated. Androgens produced by the testes thus appear to modify the animals’ response to urinary odours, though the effect is partly confounded with those of experience. As in females, genital sensitivity in male rats is increased by sex steroids. Testosterone causes the skin of the glans penis to become thinner so that underlying sensory cells receive more stimulation and the male can respond more effectively to the copulatory movements of the female. Conversely, castration results in loss of the surface papillae of the glans, with a concomitant reduc-tion in sensitivity and copulatory behaviour.

3.3.1.3 Effects on effector systems

Animals use a range of appendages and other external structures in performing different behaviours. Various hormones affect the development of such structures and thus their efficacy in performing whatever behaviours depend on them. In some cases, hormones induce appropriate muscle development, as in the hypertrophied brachial musculature used by male frogs in amplexus (coupling). The aminergic neurotransmitters serotonin and octopamine in lobsters (Homarus vulgaris) prime receptors in muscles of the exoskeleton to respond appropriately to particular stimuli. Serotonin primes the postural muscles for flexion, for example when another lobster comes into view, while octopamine inhibits flexion. Together, they help coordinate dominant and subordinate responses to social stimuli (Kravitz 1988). Sex differences in call characteristics in the clawed toad, Xenopus laevis, are also due to hormonal effects on muscle development. In this case, androgens increase the number of muscle fibres in the larynx of males as they mature, and stimulate the development of more so-called ‘fast twitch’ fibres that produce the characteristic rapid trill of the male call (Kelley & Gorlick 1990). In women, changing oestrogen and progesterone levels during the menstrual cycle affect the strength of several muscle systems, causing fluctuations in physical performance at different stages of the cycle (Reilly 2000).

Secondary sexual adornments provide other examples of hormonally induced effector systems. In newts, prolactin appears to be important in the development of the enlarged tail fin in males, which is used to fan a stream of water at the female during courtship.

While prolactin also influences the vigour of tail fanning, there is a synergistic effect with growth hormone in enhancing the overall performance of the response (Toyoda et al.

1992). Sexually selected plumage characteristics in birds provide other examples.

These range from minor markings, such as the orange patch in the cap of male gold-crests (Regulus regulus), to elaborate, gaudy structures such as the tails of male birds of paradise, or the combs and wattles of male fowl. In many species, the development and maintenance of secondary sexual characters depend on sex steroids, in some cases the presence of androgen, in others the absence of oestrogen (Owens & Short 1995;

Kimball & Ligon 1999; Fig. 3.30). For example, comb and wattle size in newly hatched male and female domestic chicks can be increased to proportions normally found in sexually mature males by injecting testosterone, while castration of mature males results in a pronounced reduction of comb and wattle size. Plumage dimorphism in birds of this group (galliforms), as in ratites (ostriches, rheas, etc.) and anseriforms (ducks, geese, etc.), on the other hand, depends on the presence or absence of oestrogen. Secretion of oestrogen leads to dull plumage typical of females, while an absence of the hormone leads to bright male-like plumage. Removal of the gonads in either sex results in

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the bright plumage typical of males. Among passerines (perching birds such as sparrows and finches), bright male plumage depends on secretion of luteinising hormone, and gonadectomy has no effect on the development of plumage colouration (Kimball &

Ligon 1999; Fig. 3.30).

Horn and antler size in artiodactyls (cloven-hoofed mammals) such as deer and gazelle, often an important determinant of success in intermale disputes and mate attrac-tion (see Chapter 10), appears to be at least partly determined by androgen levels. In addition, sexual behaviour in mammals may be mediated by hormonal effects on odour production. Oestrogen administered intravaginally to female rhesus monkeys (Macaca mulatta) increases the tendency for males to mount or press a lever to gain access to a female, the latter effect disappearing when males are rendered anosmic (Michael &

Keverne 1968; Michael & Saayman 1968).

3.3.1.4 Effects on development

Hormones have a profound effect on the development of young animals and impart characteristic features to their behaviour as adults. While hormonal effects on behaviour and associated physiological processes in adults are usually reversible and independent of age (once adult), those affecting development are permanent and irreversible, often limited to clearly defined periods in the developmental process, and usually manifested later in life rather than at the time of effect (Beach 1975). For example, hormone-mediated Figure 3.30 Plumage dimorphism in eider ducks (Somateria mollissima) and pied flycatchers (Ficedula hypoleuca). Although ducks and passerines often show similar degrees of dimorphism, bright plumage in males of the two groups depends on very different hormonal influences. See text.

anatomical and physiological changes are important in the development of sexual behaviour. In guinea pigs, testosterone levels influence the development of the genitalia, so that female offspring born of females treated with testosterone proprionate during pregnancy have male-like genitals. If they are then ovariectomised and treated with gonadal hormones, these offspring develop more male-like behaviour than controls whose mothers were not treated with testosterone (Young 1965).

Male and female rats are born with a CNS that is largely undifferentiated with respect to sexual behaviour, though with a tendency towards a characteristically female pattern (Harris & Levine 1965). Differentiation of male behaviour is brought about by the later action of testosterone. If female rats are given testosterone at around 4 days of age, their oestrous cycle and sexual behaviour as adults are suppressed and remain unresponsive to ovariectomy and oestrogen treatment. Similarly, treatment of 4-day-old males with oestrogen results in some loss of sexual responsiveness through partial functional castration and impaired development of the penis.

Studies of a range of species suggest that hormonal effects on sexual responses such as those above occur during more or less clear-cut critical periods in an animal’s develop-ment. Sometimes the critical period is prenatal, sometimes postnatal. While guinea pigs and rats exemplify these respective conditions, the critical period in guinea pigs, which are more precocial (born at a later stage of development), in fact occurs at the same developmental stage as in rats. However, there is evidence that hormonal influences are at work rather earlier than the critical period suggested by experimental manipulations.

In both rats and mice, for example, the sex of neighbouring foetuses in utero may have a marked effect on female genital morphology and sexual behaviour as a result of testicular androgens being synthesised and released late in gestation (Clemens 1974; vom Saal 1989). Other evidence from birds suggests that hormonal influences on development may not always be restricted to a sharply defined critical period, and that behavioural effects can occur at different times during development (Schumacher et al. 1989).

Prenatal hormonal influences in mammals can have more profound effects on neural development and behaviour. Thyroxin deficiency in human mothers is known to be associated with deficits in motor and cognitive functions in subsequent offspring. Rats born to thyroid-deficient dams also show marked behavioural deficits, including reduced learning ability and responsiveness to emotionality and open field tests. These effects are associated with reduced levels of the cortical neurotransmitters influencing activity, mood and learning in animals with normal thyroid function (Friedhoff et al. 2000).

3.3.1.5 Factors influencing relationships between hormones and behaviour Hormones, then, have diverse effects on behaviour, both directly and indirectly. Not surprisingly, therefore, these effects can be conditional on a host of internal and external factors.

Individual genotype

Differences in individual genotype are one source of variation in response. Experiments with different genetic strains (2.3.2.2) have indicated various strain-specific effects of hormone treatment. Strains of domestic fowl, which had been selected for different tendencies to complete mating, showed very different responses to castration and sub-sequent androgen treatment: in both cases hormone treatment caused birds to resume the precastration mating behaviour typical of their strain (McCollom et al. 1971).

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Similarly, perinatal administration of androgen to female mice increased aggressive behaviour if females came from a strain in which males were typically aggressive, but had little effect if males of the strain were non-aggressive (Vale et al. 1972). Even within strains individuals show consistent differences in hormone-related behaviour.

Individual differences in copulatory behaviour among male guinea pigs, for example, were resumed after castration when animals were given the same dose of testosterone (Fig. 3.31). On a broader scale, effects of sex steroids on the development of sex-typical behaviour appears to depend on which sex is homogametic (has two sex chromosomes the same). In mammals this is the female (females XX, males XY), in birds the male (males ZZ, females ZW). As a result, the development of sexuality in the absence of steroid influence defaults to female in mammals, but male in birds. Recent evidence suggests that interactions between sex steroids and disease resistance genes may also account for some sex-typical relationships between behaviour and immune function (Klein 2000; see 3.5.2).

Seasonal variation

Seasonal effects are also important in determining behavioural responses to hormones.

In red deer (Cervus elephus), the administration of testosterone to stags in winter brings about full rutting behaviour, whereas in late spring it has no effect until the normal rutting period (Lincoln et al. 1972). Similar seasonal influences are evident in the receptivity of female anoles (Anolis carolinesis), a desert lizard, to approaches by males following ovariectomomy and oestrogen and progesterone treatment (Wu et al. 1985).

The seasonal cycling in the size of song control centre nuclei in the forebrain of canaries Figure 3.31 Individual male guinea pigs differ in their levels of sexual activity and these differences are maintained in their response to castration and hormone replacement. Solid line, ‘high drive’; dashed line, ‘medium drive’; dotted line, ‘low drive’ individuals. After Grunt & Young (1952).

(3.1.3.1, Fig. 3.12a) appears to be under the control of testosterone. Goldman &

Nottebohm (1983) showed that increase in size (recrudescence) of the HVC (Fig. 3.12a) in male canaries each spring was due to the influence of testosterone on the formation of new nerve cells. Interestingly, and in contrast to the testosterone-induced sexual dimorphism in rats (3.3.1.4), testosterone treatment induces the same pattern of develop-ment in female canaries, which then also sing. Seasonal changes in hormone levels and associated behaviour like these are widespread in animal species and can persist even when external cues to seasonality are removed under controlled laboratory conditions (see 3.4).

Effects of experience

Past experience is another factor that can have a profound influence on the behavioural effects of hormones. The maintenance of copulatory behaviour following castration in male cats, for example, is more protracted if males have previously had experience of mating.

In young male chickens, there appears to be an interaction between prior copulatory experience and treatment with male and female sex steroids in the lateralisation of copulatory control in different cerebral hemispheres. Using eye patches to restrict vision to one eye, and treating birds with 5-alpha-dihydrotestosterone (5-alpha-DHT) or oestradiol, Bullock & Rogers (1992) found that different hemispheres played a role in copulatory activity depending on which eye was covered. However, once patches had been swapped between eyes, treatment with 5-alpha-DHT led to high copulation scores regardless of which eye was covered, suggesting the hormone facilitated either inter-ocular transfer of behavioural control (i.e. transfer from the part of the brain served by one eye to the part served by the other), or equal access of both eyes to the regions of the brain which control copulation (Bullock & Rogers 1992).

Experience can itself lead to changes in hormonal state, emphasising the frequent bidirectionality of relationships between behaviour and hormonal changes. In male squirrel monkeys (Siamiri sciureus), testosterone levels prior to grouping did not pre-dict the social rank a male subsequently adopted (Fig. 3.32). Once rank relationships were established, however, there was a close correlation between rank and testosterone concentration, with the alpha (top ranking) male having the highest testosterone con-centration and the gamma (lowest ranking) the lowest (Mendoza et al. 1979). The

3.3 ⁿ Hormones and behaviour x ₁₅₁

Figure 3.32 Mean levels of testosterone in male squirrel monkeys (Siamiri sciureus) in relation to their social status in different social environments. See text. After Mendoza

Figure 3.32 Mean levels of testosterone in male squirrel monkeys (Siamiri sciureus) in relation to their social status in different social environments. See text. After Mendoza