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Neural Mechanisms Underlying Sex-Specific Behaviors in Vertebrates Dulac and Kimchi 677

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Neural Mechanisms Underlying Sex-Specific Behaviors in Vertebrates Dulac and Kimchi 677 Neural mechanisms underlying sex-specific behaviors in vertebrates Catherine Dulac and Tali Kimchi From invertebrates to humans, males and females of a given eggs are spawned will the male release its sperm and species display identifiable differences in behaviors, mostly but fertilize the eggs. In other species such as frogs, croco- not exclusively pertaining to sexual and social behaviors. Within diles, and songbirds, males produce an intense male- a species, individuals preferentially exhibit the set of behaviors specific courtship song that entices the female to enter that is typical of their sex. These behaviors include a wide range their territory and pick them as mate, while in rodents, of coordinated and genetically pre-programmed social and intense olfactory investigation leads to male- and female- sexual displays that ensure successful reproductive strategies specific sexual behaviors. Other social sex-specific beha- and the survival of the species. What are the mechanisms viors in rodents include male–male and lactating female underlying sex-specific brain function? Although sexually aggressive behaviors, and parental behavior in which dimorphic behaviors represent the most extreme examples of females of most species invest significantly more time behavioral variability within a species, the basic principles in taking care of the offspring. Thus, each species has underlying the sex specificity of brain activity are largely evolved discrete communication strategies and behavior unknown. Moreover, with few exceptions, the quest for responses enabling individuals of each sex to identify fundamental differences in male and female brain structures each other, to successfully breed and to care for their and circuits that would parallel that of sexual behaviors and progeny. The study of developmental and neural mech- peripheral organs has so far uncovered modest quantitative anisms controlling sexually dimorphic brain function has rather than the expected clear qualitative differences. As will be been the topic of a vast amount of research, leading to the detailed in this review, recent advances have directly identification of gonadal hormones as a major player in the challenged the established notion of the unique role of steroid establishment of sex-specific brain function. Moreover, hormones in organizing and activating male- and female- these earlier studies uncovered discrete neuronal circuits specific brain circuits and have uncovered new mechanisms and nuclei underlying sex-specific responses, and pointed underlying the neural control of sex-specific behaviors. to the central role of the vomeronasal pathway in govern- ing the sensory control of sexual behavior. Address Department of Molecular and Cellular Biology, Howard Hughes Medical The role of sex hormones Institute, Harvard University, Cambridge, MA 02138, USA Arnold Adolph Berthold first investigated the role Corresponding author: Dulac, Catherine ([email protected]) played by gonadal hormones in establishing sex-specific behavior. Berthold hypothesized that intact testes are necessary for the development of male-typical charac- Current Opinion in Neurobiology 2007, 17:675–683 teristics, leading him to conduct a series of experiments using castration and testes replacement in roosters. He This review comes from a themed issue on Neurobiology of Behaviour found that males castrated as juveniles later showed Edited by Edvard Moser and Barry Dickson deficits in adult behaviors such as aggression, mating and crowing. These castrated animals also failed to develop the large size and the plumage characteristics 0959-4388/$ – see front matter of normal males. Furthermore, Berthold discovered that # 2008 Elsevier Ltd. All rights reserved. the effects of castration could be reversed if the sub- ject’s testes, or the testes of another male, were DOI 10.1016/j.conb.2008.01.009 implanted into the body cavity of a castrated juvenile, giving the first indication that hormones secreted by the gonads play a crucial role in the organization of sexually Historical perspective dimorphic behaviors [2]. The mating behavior of the three-spined stickleback represents one of the best described examples of chain A series of experiments on guinea pigs performed by reactions of sex-specific interactions [1]. The male stick- William Caldwell Young confirmed the crucial role played leback initiates a zigzag courtship dance when detecting by gonadal hormones in establishing the basic pattern of the presence of a pregnant female. The female reacts to reproductive behavior [2–4]. Young demonstrated that the red color of the male by swimming aside, inducing perinatal exposure of female guinea pigs to elevated the male to lead the female to its nest. The presence of androgens permanently suppressed their capacity to dis- the female in the nest releases a trembling behavior by play feminine sexual behavior (defeminization) and sig- the male, which leads to female spawning. Only after the nificantly enhanced their display of masculine sexual www.sciencedirect.com Current Opinion in Neurobiology 2007, 17:675–683 676 Neurobiology of Behaviour behavior (masculinization). From these behavioral results as components of the vomeronasal system, a sensory it was suggested that the exposure to prenatal androgens system thought to process pheromone information and had permanently altered the brain structures underlying required for sexual and aggressive responses [12–14]. sexual behavior and that, similar to the development of peripheral sexual organs, androgens ‘organized’ the The central role of the vomeronasal pathway developing nervous system at a crucial period of early In rodents, pheromone detection is essential for triggering development [5]. innate sexually dimorphic responses (reviewed in refer- ences [18,19]). For example, in males, female phero- These findings led to the proposal that gonadal hormones mones lead to testosterone and LH surges, puberty have a dual role in the organization and activation of acceleration as well as initiation of immediate behavioral sexually dimorphic brain circuits. According to this model, responses such as courtship display, ultrasound vocaliza- exposure, or lack of exposure, to androgens and to their tions, and copulatory behavior. By contrast male phero- estrogen metabolites during a crucial period of perinatal mones can delay puberty onset of other males and development leads to the differential organization of the promote conspecific male–male aggression and territori- neural pathways that underlie male- and female-specific ality scent marking. In females, male pheromones can behaviors. This perinatal hormonal activity permanently accelerate puberty onset (Vandenbergh effect), block modifies the ability to manifest certain sexually dimorphic pregnancy (Bruce effect), induce estrous cycle (Whitten behaviors in adulthood. In turn, differential exposure to sex effect) and sexual receptivity (lordosis behavior), while steroid hormones at puberty activates the pre-established group-housed female pheromones lead to puberty delay male- and female-neural circuitry leading to sex-specific and estrous cycle inhibition. Other female-typical beha- reproductive and social displays. viors such as maternal aggression, nesting and pup retrie- val, were also shown to be mediated by pheromones. Sexually dimorphic brain areas The discovery of the organizational effect of steroid From these results, the VNO emerged as a structure hormones led to an extensive quest for target brain nuclei essential for pheromone detection, and responsible for undergoing ‘masculinization’ and ‘defeminization’ in the activation of innate sexually dimorphic reproductive young males in order to generate the effective control behavioral and endocrine responses in males and females. centers of sex-specific behaviors such as mating and courtship in the adult [6]. Recent studies have challenged some of the prevailing hypotheses described above and have shed new light on Initial clues were obtained by Goy and Phoenix [7] who mechanisms thought to underlie the organization and the found that destruction of brain tissue lying in the mid- activation of sexual dimorphic traits in vertebrates. ventral region of the hypothalamus resulted in a signifi- cant decrease in sexual receptivity in female guinea pigs. In male rats extensive injury to the neocortex results in a Gonadal sex hormones versus genomic decreased tendency to copulate [8], whereas similar information lesion in females produced no significant change in sexual In birds and mammals sexual differentiation is primarily behavior [9]. promoted by two mechanisms: Surprisingly, in rodents, only a limited number of brain 1. The differentiation of sex-specific gonads is deter- structures were found to exhibit clear sexual dimorphism mined by the function of sex chromosome genes. In despite the striking differences in behavior between the mammals, the presence or absence of the testis- sexes. In rats these include the sexual dimorphic nucleus determining gene SRY, directs the undifferentiated of the preoptic area (SDN-POA) and the posterodorsal gonad to form a testis that produces testicular medial amygdala (MePD), both of which are larger in hormones. The timing and level of SRY expression males than females, and the anteroventral periventricular in males must occur in a narrow window during gonad nucleus (AVPV), which is larger in females than in males development in order to activate the male pathway [10,11]. Subtle sex differences in levels of neurotransmit- [20]. In
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