Lesions of the posterior bed nucleus of the stria terminalis eliminate opposite‐sex odor preference and delay copulation in male Syrian hamsters: role of odor volatility and sexual experience

Abstract

In Syrian hamsters (Mesocricetus auratus), the expression of reproductive behavior requires the perception of social odors. The behavioral response to these odors is mediated by a network of ventral forebrain nuclei, including the posterior bed nucleus of the stria terminalis (pBNST). Previous studies have tested the role of pBNST in reproductive behavior, but the use of large, fiber-damaging lesions in these studies make it difficult to attribute post-lesion deficits to pBNST specifically. Thus, the current study used discrete, excitotoxic lesions of pBNST to test the role of pBNST in opposite-sex odor preference and copulatory behavior in both sexually-naïve and sexually-experienced males. Lesions of pBNST decreased sexually-naïve males' investigation of volatile female odors, resulting in an elimination of opposite-sex odor preference. This elimination of preference was not due to a sensory deficit, as males with pBNST lesions were able to discriminate between odors. When, however, subjects were given sexual experience prior to pBNST lesions, their preference for volatile opposite-sex odors remained intact post-lesion. Similarly, when sexually-naïve or sexually-experienced subjects were allowed to contact the social odors during the preference test, lesions of pBNST decreased males' investigation of female odors, but did not eliminate preference for opposite-sex odors, regardless of sexual experience. Finally, lesions of pBNST delayed the copulatory sequence in sexually-naïve, but not sexuallyexperienced, males such that they took longer to mount, intromit, ejaculate, and display long intromissions. Together, these results demonstrate that pBNST plays a unique and critical role in both appetitive and consummatory aspects of male reproductive behaviors.

The bed nucleus of the stria terminalis is critical for sexual solicitation, but not for opposite-sex odor preference, in female Syrian hamsters

“…These results were unexpected, given that in male hamsters, similar lesions of BNST completely eliminate opposite-sex odor preference (Been and Petrulis, 2010), and larger, electrolytic lesions of BNST decrease investigation of female hamster vaginal secretion (Powers et al, 1987). Moreover, both males and females require a functional MA, the major input structure for BNST, for odor preference (Maras and Petrulis, 2006; Petrulis and Johnston, 1999), and both sexes show similar neural responses to opposite-sex odors in MA (DelBarco-Trillo et al, 2009; Maras and Petrulis, 2010; Meredith and Westberry, 2004) and BNST (Hosokawa and Chiba, 2007; Maras and Petrulis, 2010).…”

“…There are known anatomical and functional differences between the anterior and posterior divisions (Dong et al, 2001). For example, the posterior division of BNST is more heavily interconnected with MA, and has been implicated in the control of reproductive behaviors (Been and Petrulis, 2010; Wood, 1998). Although it also receives some input from MA, the anterior division is more strongly interconnected with the central nucleus of the amygdala and appears to be involved in anxiety and stress responses (Davis and Shi, 1999).…”

“…BNST receives input from the olfactory system both directly (Davis et al, 1978), as well as indirectly via MA and other amygdaloid nuclei (Coolen and Wood, 1998; Wood and Swann, 2005) and in male hamsters, lesions of BNST eliminate opposite-sex odor preference (Been and Petrulis, 2010). In female hamsters, large bilateral electrolytic lesions of the medial preoptic area (MPOA) that also damage BNST decrease vaginal marking in response to males (Malsbury et al, 1977).…”

Dissociated functional pathways for appetitive and consummatory reproductive behaviors in male Syrian hamsters

“…Lesions of MPOA eliminate preference for volatile opposite-sex odors (Been and Petrulis, 2010b) and severely impair or eliminate copulatory behavior in male hamsters (Been and Petrulis, 2010b) and nearly every vertebrate species studied to date (Hull et al, 2002). In comparison, lesions of BNST eliminate male hamsters’ preference for volatile opposite-sex odors and decrease investigation of directly contacted female odors (Been and Petrulis, 2010a), without causing dramatic changes in copulatory behavior in male hamsters and other rodents (Been and Petrulis, 2010a; Claro et al, 1995; Liu et al, 1997). MA, BNST, and MPOA each contain dense populations of steroid-sensitive neurons (Wood et al, 1992; Wood and Newman, 1995a) and site-specific implants of testosterone into either MA or BNST/MPOA restore reproductive behavior in castrated males (Wood and Newman, 1995c).…”

“…To test these hypotheses, we used the asymmetrical pathway lesion technique to functionally disconnect MA from either MPOA (MAMPOA-X) or BNST (MA-BNST-X). This technique takes advantage of the primarily ipsilateral connections between MA, BNST and MPOA (Kevetter and Winans, 1981; Simerly and Swanson, 1986; Wang and Swann, 2006; Wood and Swann, 2005) and the finding that unilateral lesions of MA (Maras and Petrulis, 2006), BNST (Been and Petrulis, 2010a), or MPOA (Been and Petrulis, 2010b) do not disrupt odor preference or copulation in male Syrian hamsters. Thus, unilateral lesions of two of these nuclei in contralateral brain hemispheres (CONTRA) result in a functional disconnection , in which two nuclei within a hemisphere are prevented from communicating with each other, but a sufficient amount of each nucleus to generate behavior remains.…”