Understanding and Preventing Violence, Volume 2: Biobehavioral Influences (1994)
Chapter: STUDIES ON NONPRIMATES
EARLY PROGRAMMING EFFECTS OF HORMONES
STUDIES ON NONPRIMATES
The frequently recorded sex differences in aggressiveness (see Brain, 1979b) in a variety of situations may reflect variations in the early patterns of endogenous sex steroid secretion and/or adult production of hormones. Androgens have developmental effects in early life when they alter the capacity of the animal to react aggressively in adulthood (Leshner, 1981). The presence of androgens in the mature animal is also a necessary prerequisite for the display of this form of behavior. Dixson (1980) stated that the neural mechanisms that mediate patterns of sexual and aggressive behavior in rodents are profoundly masculinized and defeminized by the influences of androgens on the developing brain (note that masculinization and defeminization are different processes). Male or androgenized but genetically female rats (Rattus norvegicus) not only need higher doses of estrogen to produce female-typical sexual responses (e.g., lordosis) than nonmasculinized females (van de Poll and van Dis, 1977), but also fail to respond to testosterone by showing this behavior (van de Poll et al., 1978). The vast majority of studies relating neonatal hormone applications to adult aggressive behavior have employed traditional "aromatizable" androgens (i.e., those that can be metabolized to estrogens in target tissues including the CNS). Male rats and house mice (Mus musculus domesticus) show a greater potential for aggressiveness than female counterparts because endogenous hormone secretion by the testis occurs earlier than that by the ovary. The early surge of testosterone was said to "create" the neural circuitry of male rodents from the "undifferentiated" (female) condition. Recently revealed complications in this process are considered in Aron et al. (1990), Brain and Haug (1990), and Goy and Roy (1990).
Many authors have found that testosterone propionate treatment of neonatally castrated male (vom Saal et al., 1976) and female (Mugford, 1974) mice results in these animals showing much higher incidences of fighting in adulthood than counterparts treated with control injections. It seem reasonable to conclude that (in rodents at least) testosterone plays an important role in the genesis and maintenance of some forms of aggressive behavior. One should note, however, that in some species and situations, no sex differences in testosterone-mediated aggression are apparent. This is certainly and pertinently true of same-sex encounters in certain strains of rats (van de Poll et al., 1981).
TABLE 1 Synopsis of the Effects of Early Treatments with Aromatizable Androgens (e.g., testosterone (T) and androstenedione) on Social Conflict
|
Class |
Species |
References |
Effects |
|
Pisces |
Xiphophorus variatus (platyfish) |
Laskowski, 1954 |
Augments in female |
|
Aves |
Gallus domesticus (chicken) |
Andrew, 1975 |
Augments in male |
|
|
Anas platyrhynchos (domestic duck) |
Balthazart and Stevens, 1975 |
Augments in male |
|
Mammalia |
Mouse |
Edwards, 1968, 1969, 1971 |
Augments in ovariectomized, T-treated female |
|
|
Mesocricetus auratus (golden hamster) |
Payne, 1976 |
Augments in gonadectomized, T-treated males and females |
|
|
Macaca mulatta (rhesus monkey) |
Joslyn, 1973 |
Augments in female |
The fact that early exposure to testosterone (or other aromatizable androgens) increases aggressiveness in a wide range of nonhuman species in emphasized in Table 1. There are considerable species differences in the roles of hormones influencing prepubertal aggressive behavior (Brain, 1978), with the data suggesting that lower vertebrates (such as fish, reptiles, and rodents) are more likely to show hormonal dependence than subjects such as dogs and primates. Although this may be interpreted as a phylogenetic change, one should caution that the longer life span of the less hormonally dependent species may play a role. Certainly primates are more likely to have acquired a range of social experiences before castration or steroid hormone treatment than are rats and mice.
There have been some truly excellent studies on the intrauterine location phenomenon that have added greatly to our knowledge (see review by vom Saal, 1990). The positioning of the fetus during intrauterine development is an important source of variation in the hormonal titers to which both developing male and female rats and mice are exposed. Vom Saal and Bronson (1980) found that fetuses of male mice on day 17 of gestation have three
