Benefit 1 Greater Experimental Control

Animal studies permit experimental manipulations that are not possible in humans. As a result, animal models have yielded new discoveries about the hormones, neurotransmitters, genes, and environments associated with personality traits such as aggression and dominance.

2 TABLE 20.1. Animal Studies on the Biological Bases of Aggression and Dominance, Categorized According to Benefit

Study

Animal species and gender

Main findings

Significance for personality psychology

Primary benefit

Secondary benefit(s)

Berthold Male chickens Castrated chickens developed into

(1849/1944) nonaggressive capons, but castrated chickens reimplanted with testes in the abdomen developed into normal roosters.

Shows that the testes facilitate aggression.

Hormone manipulation (1a)

Naturalistic observation (3)

Briganti et al. Male rabbits Testosterone injections only increased (2003) aggression in high-ranking rabbits.

Shows a testosterone x social rank interaction in aggression.

Hormone manipulation (1a)

Naturalistic observation (3)

Veiga et al. Female Testosterone-treated females hatched more

(2004) starlings sons; in addition, these females gained and maintained high social rank.

Shows that testosterone influences social rank in females.

Hormone manipulation (1a)

Naturalistic observation (3)

Ferris & Adult male Hamsters injected with a vasopressin

Delville hamsters antagonist into the anterior hypothalamus

(1994) decreased in aggression.

Shows that vasopressin is associated with aggression.

Pharmacological manipulation (1b)

Delville et al. Adult male Castrated and testosterone-treated animals

(1996a) hamsters administered serotonin and vasopressin agonists in the ventrolateral hypothalamus were less aggressive than animals not administered the serotonin agonist.

Shows interaction between serotonin and vasopressin in aggression.

Pharmacological manipulation (1b)

Hormone manipulation (1a)

Nelson et al. Adult male Mice lacking gene for neuronal nitric

(1995) mice oxide synthase (nNOS- mice) were more aggressive than wild-type mice.

Identifies a gene associated with aggression.

Genetic manipulation (1c)

Chiavegatto Adult male The aggressiveness observed in nNOSet al. (2001) mice mice was caused by reduced serotonin turnover and impaired serotonin receptors.

Shows biological mechanism by which a particular gene influences aggression.

Genetic manipulation (1c)

Pharmacological manipulation (1b)

Nomura et al. (2002)

Pubertal, Male mice lacking the gene for estrogen young adult, receptor beta were more aggressive than and adult wild-type mice as adolescents and young male mice adults, but not as adults.

Adult male Male mice lacking the gene for estrogen mice receptor alpha were less aggressive than wild-type mice, despite having average testosterone levels.

De Jonge et Female Piglets raised in a poor environment were al. (1996) piglets, babies more aggressive as adults than piglets to adults raised in an enriched environment.

Newman et Male rhesus Monkeys with low activity of the monoa-

al. (2005) monkeys (3-5 mine oxidase A (MAO-A) gene that were years old) mother-reared were more aggressive.

Oliveira et al. Adult male Fish watching a fight rose in testosterone,

(2001) cichlid fish relative to those that did not watch a fight.

Delville et al. Adult male Vasopressin receptor binding in the

(1996b) hamsters ventrolateral hypothalamus disappeared in castrated animals, but not in testosterone-treated animals; vasopression microinjections did not increase aggression in castrated animals, but did increase aggression in testosterone-treated animals.

DeLeon et al. (2002)

Adolescent Anabolic-androgenic steroid treatment male hamsters during adolescence increased vasopressin binding and aggression.

Shows gene x age interaction affecting aggression.

Genetic manipulation (lc)

Hormone manipulation (la)

Identifies gene associated with aggression, and suggests that the mechanism of action is not testosterone-dependent.

Shows that early environmental conditions influence adult aggression.

Shows a genotype x early rearing environment interaction in aggression.

Shows an environmental influence on testosterone levels, which in turn may influence dominance and aggression.

Suggests a vasopressin-receptor-dependent mechanism by which testosterone influences aggression.

Genetic manipulation (lc)

Environmental manipulation (Id)

Environmental manipulation (Id)

Hormone measurement (2c)

Environmental Longitudinal study manipulation (Id) (4)

Gene promoter sequence variation (2c)

Hormone measurement (2c)

Hormone receptor Hormone binding measurement manipulation (la) (2a)

Suggests a vasopressin-receptor-dependent mechanism by which anabolic steroids influence aggression.

Hormone receptor binding measurement (2a)

Hormone manipulation (la)

(continued)

Study

Animal species and gender

Main findings

Filipenko et Adult male al. (2002) mice

Social defeat resulted in greater expression of serotonin transporter (SERT) and MAO-A messenger RNA (mRNA).

Pinna et al. Female mice Testosterone therapy increased aggression (2005) and decreased mRNA expression for 5-

alpha reductase type 1.

Wingfield et al. (1990)

Birds

Testostosterone rose to facilitate intermale competition.

Virgin & Sapolsky (1997)

Muller &

Wrangham

Male baboons

Adult male chimpanzees

Subordinate individuals that were aggressive after losing a fight had lower Cortisol levels than subordinates that were not aggressive after losing a fight.

Testosterone levels and aggression were higher in dominant individuals.

Muehlenbein Adult male Testosterone levels were correlated with et al. (2004) chimpanzees social rank.

Holekamp & Adult male Testosterone levels were higher in

Smale (1998) hyenas immigrant than in natal males;

testosterone levels correlated with social rank among immigrant males.

Significance for personality psychology Primary benefit Secondary benefit(s)

Shows an environmental influence on gene expression, which may in turn influence aggression.

Suggests that testosterone influences gene expression and aggression.

Shows that natural increases in testosterone facilitate aggression only during social instability.

Shows a relationship between Cortisol levels and aggression.

Shows a relationship between testosterone levels and aggression, as well as between testosterone levels and social rank.

Shows a relationship between testosterone levels and social rank. Shows a relationship between testosterone levels and social rank.

Gene expression measurement (2b)

Gene expression measurement (2b)

Naturalistic observation (3)

Environmental manipulation (Id)

Hormone, pharmacological, and environmental manipulations (la,lb,Id)

Hormone measurement (2c)

Naturalistic observation (3)

Naturalistic observation (3)

Hormone measurement (2c), personality and health (5)

Hormone measurement (2c)

Naturalistic observation (3)

Naturalistic observation (3)

Hormone measurement (2c)

Hormone measurement (2c)

Adkins-Regan Female zebra (1999) finches

Wommack et Male al. (2003) hamsters

Wommack & Male Delville hamsters

Mejia et al. Male and (2002) female mice

Granger et al. Male mice (2001)

Tuchscherer et al. (1998)

Male and female pigs

Neonatal estradiol plus adult testosterone treatment increased aggression.

Social subjugation during adolescence accelerated the development of aggression.

Individual differences in coping response during social subjugation in adolescence predicted the development of aggression.

A prenatal pharmacological inhibition of MAO increased aggression in adulthood.

High-aggression mice exposed to a postnatal immune stressor were less aggressive as adults.

Socially dominant pigs had better immune function than socially subordinate pigs.

Shows that neonatal and adult hormone exposure influence adult aggression.

Shows an environmental influence during adolescence on the development of aggression.

Shows an individual difference x social environment interaction in the development of aggression.

Shows a relationship between prenatal biological environment and adult aggression.

Shows an early temperament x biological environment influence on adult aggression.

Shows a relationship between social dominance and immune function.

Longitudinal study

Longitudinal study

Longitudinal study

Longitudinal study

Longitudinal study

Personality and health (5)

Hormone manipulation (1a)

Environmental manipulation (1d)

Environmental manipulation (1d), hormone measurement (2c)

Pharmacological manipulation (1b)

Environmental manipulation (1d), personality and health (5)

Naturalistic observation (3)

Veenema et Young adult Long-attack-latency mice had higher stress al. (2004) male mice responsivity than short-attack-latency

Shows a relationship between aggression and stress reactivity.

Personality and health (5)

Environmental manipulation (1d), gene expression measurement (2b)

Note. The numbers and letters in the "Primary benefit" and "Secondary benefit(s)" columns refer to the numbers and letters of subheads in the text section "The Benefits of Animal Research."

a. Hormone Manipulation

The ability to manipulate the presence or absence of hormones in animals has existed for a long time. The first formal endocrinology experiment was conducted in roosters by Arnold Berthold (1849/1944). Berthold found that when chickens were castrated during development, they developed into docile capons instead of normal roosters. These capons refrained from fighting with other males and failed to exhibit mating behavior. However, if the castrated capons were implanted with testes from other birds, they developed into normal roosters. Berthold had discovered the effect of the hormone we now know as testosterone on aggression and sexual behavior.

Hormone manipulations continue to be used today. Through techniques such as castration, injection, or capsule implantation, researchers are able to systematically study the relationships among hormones, biological processes, and behavior. In one recent study, rabbits were injected with subcutaneous testosterone propionate or a control substance (Briganti, Seta, Fontani, Lodi, & Lupo, 2003). All testosterone-treated rabbits increased in marking, digging, and defensive behaviors, but only the highest-ranking rabbits in each social group increased in aggressive behavior. This study showed that testosterone has an effect on aggression in rabbits, but that the effect is moderated by social rank.

In another study, female starlings were implanted with testosterone and placed back in their natural setting (Veiga, Vinuela, Cordero, Aparicio, & Polo, 2004). The testosterone-implanted females hatched more sons than the control females for up to 3 years after the treatment. In addition, the testosterone-treated females seemed to gain and maintain high social rank. These results suggest that the testosterone level of the mother has a direct impact on sex differentiation in offspring. In addition, testosterone may influence dominance among female starlings.

b. Pharmacological Manipulation

Advances in pharmacology have allowed scientists to develop synthetic chemicals that can either enhance (agonists) or block (antagonists) the functioning of neurotransmitters (e.g., serotonin) and hormones (e.g., testosterone) in animals. Such drugs have helped researchers examine the specific mechanisms by which neurotransmitters and hormones affect aggression and dominance.

In one study, hamsters injected with a vasopressin antagonist into the anterior hypothalamus decreased in aggression (Ferris & Delville, 1994), suggesting that vasopressin plays a role in the expression of aggressive behavior. In a follow-up study, researchers castrated hamsters and treated half of them with testosterone (Delville, Mansour, & Ferris, 1996a). Next, the researchers injected fluoxetine (a serotonin agonist) or vehicle (a control substance) into the testosterone-treated hamsters. Finally, vasopressin was injected into all testosterone-treated animals. The researchers found that fluoxetine inhibited the effects of vasopressin on aggression, indicating that serotonin may inhibit aggression by blocking vasopressin functioning.

Such studies demonstrate how pharmacological manipulations can be used to understand the biological mechanisms underlying individual differences in aggression and dominance. Moreover, the second study (Delville et al., 1996a) shows how a pharmacological manipulation (the serotonin agonist fluoxetine) can be combined with hormone manipulations (testosterone and vasopressin manipulations) to examine the interplay between neurotransmitters and hormones. Future research in animals is likely to combine multiple methodologies (e.g., genetic, hormone, and pharmacological manipulations) to test complex models of the relationships among genes, neurotransmitters, hormones, and environments. Personality psychologists can profit from such powerful methodologies.

c. Genetic Manipulation

Technological advances in molecular biology allow animal researchers to remove particular genes from, or insert them into, an animal's DNA. At this time the genetics of laboratory mice are relatively well understood, making them the primary target of genetic manipulation studies. Both knockout mice (those missing a specific gene) and transgenic mice (those in which a gene has been inserted) have been used to investigate the effects of genes on personality traits.

In one study, knockout mice lacking the gene for neuronal nitric oxide synthase (nNOS- mice) were more aggressive than wild-type (normal) mice (Nelson et al., 1995). This result suggests that nNOS is important for inhibiting aggression. A subsequent knockout study using nNOS- mice found that the increased aggression in the knockout mice could be attributed to disrupted serotonin functioning (Chiavegatto et al., 2001), suggesting that the effects of nitrous oxide on aggression was mediated by an impairment in serotonin.

In another study, researchers were interested in examining the effects of the estrogen receptor alpha gene on aggression (Ogawa, Lubah, Korach, & Pfaff, 1997). Previous research in mice had discovered that one pathway by which testosterone leads to aggression is through conversion into the hormone estradiol via the enzyme aromatase (e.g., Bowden & Brain, 1978). To find out which specific estrogen genes were involved, the scientists compared knockout mice lacking the gene for estrogen alpha receptors to wild-type mice. The knockout mice had average testosterone levels, but were less aggressive than the wild-type mice (Ogawa et al., 1997). These results suggest that the reduction in aggression was not due to reductions in testosterone, but rather to a disruption in estrogen receptor alpha functioning.

Together, these two studies show how discoveries regarding the relationships between genes and personality traits can be made by using knockout mice models. Such genetic manipulation studies suggest that the genes for nNOS and estrogen receptor alpha, along with several others (e.g., the monoamine oxidase A [MAO-A] gene, Cases et al., 1995; the serotonin 1B [5-HT1B] receptor gene, Saudou et al., 1994) play a role in aggression. Because genes cannot be manipulated in humans, animal models afford unique opportunities to illuminate the genetic underpinnings of personality.

d. Environmental Manipulation

Relative to human researchers, animal researchers are able to exercise greater control over the environments of their subjects. Thus animal studies provide excellent opportunities to examine the role of environmental factors, such as rearing practice, in personality development. For example, in a study of female piglets, those individuals raised in poor environments (an indoor farrowing crate) were more aggressive as adults than individuals raised in enriching environments (an outdoor pasture with a half-open farrowing crate; De Jonge, Bokkers, Schouten, & Helmond, 1996). In a study of rhesus macaques, mother-reared individuals had higher social ranks as adults than peer-reared individuals (Bastian, Sponberg, Sponberg, Suomi, & Higley, 2003). Such experimental animal studies may inform our understanding of how early environments affect personality development in humans (whose rearing environments cannot be manipulated experimentally).

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