Neural mechanisms underlying sex-specific behaviors in vertebrates

Abstract

From invertebrates to humans, males and females of a given species display identifiable differences in behaviors, mostly but not exclusively pertaining to sexual and social behaviors. Within a species, individuals preferentially exhibit the set of behaviors that is typical of their sex. These behaviors include a wide range of coordinated and genetically pre-programmed social and sexual displays that ensure successful reproductive strategies and the survival of the species. What are the mechanisms underlying sex-specific brain function? Although sexually dimorphic behaviors represent the most extreme examples of behavioral variability within a species, the basic principles underlying the sex specificity of brain activity are largely unknown. Moreover, with few exceptions, the quest for fundamental differences in male and female brain structures and circuits that would parallel that of sexual behaviors and peripheral organs has so far uncovered modest quantitative rather than the expected clear qualitative differences. As will be detailed in this review, recent advances have directly challenged the established notion of the unique role of steroid hormones in organizing and activating male- and female-specific brain circuits and have uncovered new mechanisms underlying the neural control of sex-specific behaviors.

Figure 1

A bilateral gynandromorphic finch in which the right half of the body (A), gonads (B), sex-chromosome linked gene expression in the brain (C), and volume of sexually dimorphic nuclei (D) have male characteristics, while the left half is female-like. Striking sex differences have developed and are maintained in each side of the brain although they have been exposed equally to circulating gonadal hormones. This result supports the existence of cell-autonomous information provided by sex chromosome genes and independent from gonadal sex hormones (modified from Agate RJ, et al., 2003 with permission from authors).

Figure 2

According to the prevailing dogma of brain sexual differentiation, gonadal sex-hormones organize and activate hard-wired neural circuits mediating sex-specific behaviors that are distinct in the male and the female brains (A). Recent findings in the mouse suggest of a new model according to which fully functional male- and female-behavior circuits develop and are maintained in the brain of both sexes and are under the control of a sex-specific vomeronasal sensory switch (B). By adopting discrete modules of circuits specific for the opposite sex, new behavioral traits might emerge during evolution that are exhibited by the opposite sex in closely related species. One possible example of such evolution is the parental behavior of male prairie voles, which is not displayed by males of other vole species (C). Furthermore, such network organization might account for the rapid behavioral sex-reversals, as occurs in many coral-reef fishes (D) (modified from Kimchi T, et al., 2007).