Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain

Abstract

Male aggressive behavior is generally regulated by testosterone (T). In most temperate breeding males, aggressive behavior is only expressed during the reproductive period. At this time circulating T concentrations, brain steroid receptors, and steroid metabolic enzymes are elevated in many species relative to the nonreproductive period. Many tropical birds, however, display aggressive behavior both during the breeding and the nonbreeding season, but plasma levels of T can remain low throughout the year and show little seasonal fluctuation. Studies on the year-round territorial spotted antbird (Hylophylax n. naevioides) suggest that T nevertheless regulates aggressive behavior in both the breeding and nonbreeding season. We hypothesize that to regulate aggressive behaviors during the nonbreeding season, when T is at its minimum, male spotted antbirds increase brain sensitivity to steroids. This can be achieved by locally up-regulating androgen receptors (ARs), estrogen receptors (ERs), or the enzyme aromatase (AROM) that converts T into estradiol. We therefore compared mRNA expression of AR, ERa, and AROM in freeliving male spotted antbirds across reproductive and nonreproductive seasons in two brain regions known to regulate both reproductive and aggressive behaviors. mRNA expression of ER in the preoptic area and AR in the nucleus taeniae were elevated in male spotted antbirds during the nonbreeding season when circulating T concentrations were low. This unusual seasonal receptor regulation may represent a means for the year-round regulation of vertebrate aggressive behavior via steroids by increasing the brain's sensitivity to sex steroids during the nonbreeding season.

Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution

“…Behavioural independence from circulating T may permit adaptive expression of aggression that can side-step the costs of high systemic T to some degree [1,34,37]. Similar patterns appear to apply where high levels of aggression persist in the non-breeding season, despite low circulating T [38,39], and these mechanisms of aggression that relate to neural sensitivity to sex steroids may allow individuals of both sexes to express aggression somewhat independently of circulating T.…”

Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression

“…That is, mice with abundant AR in the NAcc and VTA attain higher scores on the winner index during the test encounter, indicating that these individuals have an above-average chance of winning social disputes (17,24). Thus, the experience of victory itself likely modifies the neural machinery controling social aggression (25,26), which in turn suggests that the winner effect is to some degree regulated at the level of the brain. One possibility is that increased androgen sensitivity in the NAcc and VTA primes the neuronal "reward circuitry," such that the reinforcing properties of aggressive encounters develop more readily and the resulting motivation to fight in the future becomes more pronounced.…”

Latitudinal Distribution, Migration, and Testosterone Levels in Birds

“…For example, predation may be a selective factor acting via sexual characters that can be controlled by T (e.g., Marler et al 1988;Schwabl and Kriner 1991;Saino and Møller 1995;Hunt et al 1997), because such traits are attractive to predators (e.g., Götmark and Post 1996;Møller et al 2006) and show latitude-dependent expression (Norris et al 2007). Fourth, some tropical birds may not require high T levels to mediate reproductive behavior, because they are more sensitive to low hormone levels (Hau et al 2000;Canoine et al 2007). Finally, errors in our measurements may contribute to the low explanatory power of migration and laying period.…”