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 the pBNST in reproductive behavior, but the use of large, fiber-damaging lesions in these studies make it difficult to attribute post-lesion deficits to the pBNST specifically. Thus, the current study used discrete, excitotoxic lesions of the pBNST to test the role of the pBNST in opposite-sex odor preference and copulatory behavior in both sexually-naive and sexually-experienced males. Lesions of the pBNST decreased sexually-naive 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-naive or sexually-experienced subjects were allowed to contact the social odors during the preference test, lesions of the pBNST decreased males' investigation of female odors but did not eliminate preference for opposite-sex odors, regardless of sexual experience. Finally, lesions of the pBNST delayed the copulatory sequence in sexually-naive, but not sexually-experienced, males such that they took longer to mount, intromit, ejaculate and display long intromissions. Together, these results demonstrate that the pBNST plays a unique and critical role in both appetitive and consummatory aspects of male reproductive behaviors.

Figure 1. Lesion Reconstruction

a) Coronal sections through rostral to caudal extent of pBNST showing largest (light gray) and smallest (dark gray) lesion included in the pBNST-X group. Immunohistochemical localization of NeuN protein was used to visualize cell loss in males with excitotoxic lesions (b) compared to males with SHAM lesions (c).

Figure 2. Investigation Times for Non-Contact Preference Test

a) In NVE males, lesions of pBNST eliminated preference for opposite-sex odors, whereas b) preference for opposite-sex odors remained intact in EXP males. Dissimilar letters indicate significant differences in investigation duration within lesion group, P < 0.05. * and # indicate significant differences in investigation duration between lesion groups, P < 0.05. Data expressed as mean ± standard error of means.

Figure 3. Investigation Times for Contact Preference

Lesions of pBNST significantly decreased males’ investigation of female odors in a) NVE and b) EXP males, but preference for opposite-sex odors remained intact for both groups. Dissimilar letters indicate significant differences in investigation duration within group, P < 0.05. * and # indicate significant differences in investigation duration between groups, P < 0.05. Data expressed as mean ± standard error of means.

Figure 4. Investigation Times for Odor Discriminiation Test

a) Both SHAM and pBNST-X NVE males a) habituated to repeated presentations of male odors and dishabituated to a novel female odor and b) habituated to strawberry or baby powder odors and dishabituated to a novel non-social odor. * indicates a significant decrease between the first and fourth presentations, P < 0.05, # indicates a significant increase between the fourth and fifth presentations, P < 0.05. Data expressed as mean ± standard error of means.

Figure 5. Latencies to Mating Events

In NVE subjects, pBNST-X males had significantly longer latencies to display mounts, intromissions, ejaculations, and long intromissions than SHAM males. In EXP subjects, pBNST-X and SHAM males did not differ in their latency to any mating event. * indicates significant differences between lesion groups, P < 0.05. Data expressed as mean ± standard error of means.