Lesions that functionally disconnect the anterior and posterodorsal sub-regions of the medial amygdala eliminate opposite-sex odor preference in male Syrian hamsters (Mesocricetus auratus)

Abstract

In many rodent species, such as Syrian hamsters, reproductive behavior requires neural integration of chemosensory information and steroid hormone cues. The medial amygdala (MA) processes both of these signals through anatomically distinct sub-regions; the anterior region (MeA) receives substantial chemosensory input, but contains few steroid receptor-labeled neurons, whereas the posterodorsal region (MePD) receives less chemosensory input, but contains a dense population of steroid receptors. Importantly, these sub-regions have considerable reciprocal connections, and the goal of this experiment was therefore to determine whether interactions between MeA and MePD are required for male hamsters' preference to investigate female over male odors. To functionally disconnect MeA and MePD, males received unilateral lesions of MeA and MePD within opposite brain hemispheres. Control males received either unilateral lesions of MeA and MePD within the same hemisphere or sham surgery. Odor preferences were measured using a 3-choice apparatus, which simultaneously presented female, male and clean odor stimuli; all tests were done under conditions that either prevented or allowed contact with the odor sources. Under non-contact conditions, males with asymmetrical lesions investigated female and male odors equally, whereas males in both control groups preferred to investigate female odors. Under contact conditions, all groups investigated female odors longer than male odors, although males with asymmetrical lesions displayed decreased investigation of female odors compared to sham males. These data suggest that MeA-MePD interactions are critical for processing primarily the volatile components of social odors and highlight the importance of input from the main olfactory system (MOS) to these nuclei in the regulation of reproductive behavior. More broadly, these results support the role of the MA in integrating chemosensory and hormone information, a process that may underlie social odor processing in a variety of behavioral contexts.

Figure 1

Reconstruction of coronal sections of the largest (light gray) and smallest (dark gray) extent of lesion damage in males with asymmetrical (ASYM; n = 15) or unilateral (UNI; n = 12) lesions of MeA and MePD. Sections proceed from anterior (top) to posterior (bottom) levels, with the numbers representing the distance posterior to bregma. The side (left or right) of the MeA and/or MePD lesion was randomly assigned within each lesion group.

Figure 2

Mean (±SEM) durations of odor investigation during Odor Preference tests when contact with odor sources was either prevented (A) or allowed (B) (SHAM n = 12; UNI n = 12; ASYM n = 15). Each letter type (uppercase, primed, lowercase) represents post-hoc comparisons within experimental group, and identical letters represent homologous means within each group (p > .05, pairwise comparisons with α_fw = .05). When contact with the odor sources was prevented, ASYM males investigated female and male odors equally, whereas SHAM and UNI males preferred to investigate female odors. When contact with the odor sources was allowed, all groups preferred to investigate female odors over male odors. In both stimulus conditions, all groups investigated the female and male odors longer than clean odors.

Figure 3

Mean (± SEM) durations of investigation during the habituation-dishabituation tests when contact with the odor sources was either prevented (A) or allowed (B) (SHAM n = 7; UNI n = 6; ASYM n = 7). All groups displayed decreased investigation during the fourth presentation of the male odor compared to the first presentation of the male odor (* p <.05 with α_fw = .05). All groups also displayed increased investigation during the presentation of the female odor compared to the fourth presentation of the male odor (* p < .05 with α_fw = .05). When contact with the odor sources was allowed, ASYM males investigated the female odor for less time than compared to SHAM and UNI males (# p < .05, Tukey’s B post-hoc comparisons).