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

Abstract

In many species, including Syrian hamsters, the generation of male reproductive behavior depends critically on the perception of female odor cues from conspecifics in the environment. The behavioral response to these odors is mediated by a network of steroid-sensitive ventral forebrain nuclei including the medial amygdala (MA), posterior bed nucleus of the stria terminalis (BNST) and medial preoptic area (MPOA). Previous studies have demonstrated that each of these three nuclei is required for appropriate sexual behavior and that MA preferentially sends female odor information directly to BNST and MPOA. It is unknown, however, how the functional connections between MA and BNST and/or MPOA are organized to generate different aspects of reproductive behavior. Therefore, the following experiments used the asymmetrical pathway lesion technique to test the role of the functional connections between MA and BNST and/or MPOA in odor preference and copulatory behaviors. Lesions that functionally disconnected MA from MPOA eliminated copulatory behavior but did not affect odor preference. In contrast, lesions that functionally disconnected MA from BNST eliminated preference for volatile female odors but did not affect preference for directly contacted odors or copulatory behavior. These results therefore demonstrate a double dissociation in the functional connections required for attraction to volatile sexual odors and copulation and, more broadly, suggest that appetitive and consummatory reproductive behaviors are mediated by distinct neural pathways.

Figure 1

Lesion reconstructions. Coronal sections through the rostral to caudal extent of A) MPOA, B) BNST, and C) MA showing the largest (light gray) and smallest (dark gray) unilateral lesions included in the IPSI and CONTRA groups. Measurements indicate mm relative to bregma, 3V, 3^rd ventricle; LV, lateral ventricle; OT, optic tract. Atlas images modified from (Morin and Wood, 2001). Excitotoxic lesion damage was assessed using immunohistochemical (IHC) localization of NeuN protein. Photomicrographs of NeuN IHC show representative depletion of neurons in D) MPOA, E) BNST, and F) MA. Scale bars = 200 µm.

Figure 2

Non-Contact Odor Preference. A) In the MA-MPOA-X lesion group, SHAM, IPSI, and CONTRA males all investigated female odors more than male or clean odors. B) In the MA-BNST-X lesion group, SHAM and IPSI males investigated female odors more than male or clean odors, but CONTRA males investigated female and male odors equally. Furthermore, CONTRA males investigated female odors significantly less than SHAM or IPSI males. Data presented as mean ±SEM. Different letters indicate significant differences between odor conditions, * and # indicate significant differences between lesion groups (P < 0.05).

Figure 3

Contact Odor Preference. A) In the MA-MPOA-X lesion group, SHAM, IPSI, and CONTRA males all investigated female odors more than male or clean odors. B) Similarly, in the MA-BNST-X lesion group, SHAM, IPSI, and CONTRA males all investigated female odors more than male or clean odors. Data presented as mean ±SEM. Different letters indicate significant differences between odor conditions (P < 0.05).

Figure 4

Copulatory Behavior. A) In the MA-MPOA-X lesion group, the proportion of CONTRA males displaying mounts, intromissions, ejaculations, or long intromissions was significantly lower than SHAM or IPSI males. B) In contrast, there was no difference between SHAM, IPSI, and CONTRA males in the MA-BNST-X lesion group. Data presented as mean ±SEM. * indicates significant differences between lesion groups (P < 0.05).