Elsevier

Hormones and Behavior

Volume 50, Issue 3, September 2006, Pages 477-483
Hormones and Behavior

Testicular hormone exposure during adolescence organizes flank-marking behavior and vasopressin receptor binding in the lateral septum

https://doi.org/10.1016/j.yhbeh.2006.06.006Get rights and content

Abstract

Adolescence is a period during which many social behaviors emerge. One such behavior, flank marking, is a testosterone-modulated scent marking behavior that communicates dominance status between adult male Syrian hamsters. Testosterone modulates flank-marking behavior by altering neural transmission of vasopressin within a forebrain circuit. This study tested whether testicular hormones secreted during adolescence play purely a transient activational role in the display of flank-marking behavior, or whether adolescent steroid hormone secretions also cause long-term organizational changes in vasopressin binding within brain regions underlying flank-marking behavior. We tested this hypothesis by manipulating whether testicular secretions were present during adolescent development and then tested for flank-marking behavior and vasopressin receptor binding within the flank-marking neural circuit in young adulthood. Specifically, males were gonadectomized immediately before or after adolescence, replaced with testosterone 6 weeks following gonadectomy in young adulthood, and behavior tested 1 week later. Adult testosterone treatment activated flank-marking behavior only in males that were exposed to testicular hormones during adolescence. In addition, males exposed to testicular hormones during adolescence exhibited significantly less vasopressin receptor binding within the lateral septum than males deprived of adolescent hormones, suggesting that hormone-dependent remodeling of synapses normally occurs in the lateral septum during adolescence. These data highlight the importance of gonadal steroid hormone exposure during adolescence for the organization of neural circuits and social behavior.

Introduction

Scent marking is an important form of social communication for many mammalian species (Johnston, 1973). The Syrian hamster exhibits a stereotyped form of scent marking behavior called flank marking (Johnston, 1975). Flank marking occurs when hamsters rub pigmented sebaceous glands located on their dorsal flank region against objects in their environment (Johnston, 1975). This behavior can be stimulated by the odors of conspecifics alone but is most often displayed during social encounters (Johnston, 1975). Importantly, flank-marking behavior serves to communicate dominance status between males and is essential for the maintenance of these dominance relationships (Ferris et al., 1987).

Flank-marking behavior is influenced by testosterone (T) in adult male Syrian hamsters (Johnston, 1981). Castration significantly reduces and T replacement restores flank-marking behavior (Johnston, 1981). T modulates flank-marking behavior by altering arginine vasopressin (AVP) neural transmission within a zone that extends from the posterior medial and lateral preoptic area to the posterior medial and lateral anterior hypothalamus (MPOA-AH, reviewed in Albers et al., 2002). Microinjections of AVP within this region cause dose-dependent increases in flank-marking behavior (Albers and Ferris, 1986, Ferris et al., 1988), and the presence of T further enhances these effects (Albers et al., 1988). These data suggest that T influences flank marking by altering the sensitivity or response of the MPOA-AH to AVP, possibly by increasing AVP binding. Indeed, castration reduces and T replacement restores V1a binding within the MPOA-AH continuum (Johnson et al., 1995, Young et al., 2000).

The MPOA-AH is reciprocally connected to the lateral septum (LS), bed nucleus of the stria terminalis (BST), and the periaqueductal gray (PAG). AVP microinjection into these areas also induces flank-marking behavior (Irvin et al., 1990, Hennessey et al., 1992), suggesting they are part of a flank-marking circuit in which AVP is a neurotransmitter at multiple levels. Just as T facilitates the effects of AVP injection into the MPOA-AH on flank marking, T also enhances the effects of AVP injection into the LS-BST and PAG on flank-marking behavior, although to a much lesser extent (Albers and Cooper, 1995). Thus, while these brain regions contribute to the display of flank-marking behavior, the MPOA-AH may be the primary site mediating the activational effects of T on behavior.

The factors responsible for the development of flank-marking behavior are largely unexplored. Preadolescent hamsters are capable of flank marking in response to male odors around day 22 (Ferris et al., 1996). However, levels of flank marking at this age are much lower than what is typically observed in adults (Johnston, 1981), suggesting that this behavior continues to develop during adolescence. Although increased gonadal secretions are a hallmark of adolescent development, what role testicular secretions play in the development of flank-marking behavior is not known. One possibility is that the rise in gonadal hormones during adolescence simply activates adult levels of flank-marking behavior. Alternatively, the rise in gonadal hormones during adolescence may permanently organize neural circuits to permit activation of behavior by T in adulthood. For example, gonadal hormones during adolescence organize reproductive behavior in male Syrian hamsters (Schulz et al., 2004). Males gonadectomized prior to adolescence, and therefore not exposed to gonadal hormones during this time, show long lasting deficits in adult reproductive behavior that are not reversed by prolonged T treatment and repeated sexual experience. Thus, full hormonal activation of reproductive behavior in this species requires the presence of testicular hormones during adolescence, and the effects of adolescent testicular hormones may generalize to other hormone-modulated social behaviors such as flank marking.

The current study tested the hypothesis that exposure to gonadal hormones during adolescence is necessary for the activation of flank-marking behavior by T in adulthood. We further hypothesized that exposure to gonadal hormones during adolescence influences the degree of V1a receptor binding in the brain regions regulating flank-marking behavior.

Section snippets

Animals

All animals were housed in a 14-h light–10-h dark schedule (lights off at 1300 h EST) and had ad libitum access to food (Teklad Rodent Diet No. 8640, Harlan) and water. Animals were treated in accordance with the NIH Guide for the Care and Use of Laboratory Animals, and all protocols were approved by the Michigan State University All-University Committee for Animal Use and Care.

Castrate groups: behavior

Mann-Whitney U tests were conducted to determine whether T activates flank-marking behavior in castrated resident NoT@P and T@P males. T treatment did not alter flank mark number in NoT@P males [Mann-Whitney U = 31.50, p > 0.05; Fig. 1A]. In contrast, T significantly increased flank-marking behavior in T@P males [Mann-Whitney U = 39.00, p < 0.05; Fig. 1A]. As for the intruders, a two-factor ANOVA found no effects of resident adolescent hormone status [F(1,24) = 0.02, p > 0.05] or resident T status during

Discussion

This study demonstrates that exposure to gonadal hormones during adolescence is necessary for the activation of flank-marking behavior by T in adulthood. Adult T treatment activated flank-marking behavior during a social interaction in males exposed to adolescent hormones but not in males deprived of adolescent hormones, suggesting that gonadal hormone exposure during adolescence organizes flank-marking neural circuits to allow for activation by T in adulthood.

Although the behavior of the

Acknowledgments

We thank Kaliris Salas-Ramirez, Eman Ahmed, Julia Zehr, and Joseph Lonstein for their valuable feedback on the manuscript. We thank Constance Montville Crew and Bernadette Bentley for the excellent care of our animals. This work was supported by NIH R01-MH068764 awarded to C.L. Sisk, R01MH062641 awarded to H.E. Albers, and NIH F31-MH070125 awarded to K.M. Schulz.

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