Amygdala Response to Artificial Olfactory and Chemosensory Input

In male hamsters mating behavior is dependent on sufficient androgens and chemosensory input from the main olfactory and vomeronasal systems, whose central pathways contain cell bodies and fibers of gonadotropin-releasing hormone (GnRH) neurons. Regions of the medial amygdala (vomeronasal amygdala) contain androgen receptors and differentially process chemosignals with different social implications. According to published reports of "categorical" patterns of response, conspecific chemosensory stimuli activate the anterior (MeA) and posterior (MeP) medial amygdala, while heterospecific stimuli only activate MeA, in male hamsters (and male mice). Furthermore, chemosignals with distinct social implications differentially activate the dorsal and ventral subregions of MeA and MeP (MeAd/v, MePd/v). In sexually-naïve male hamsters, lesions of the vomeronasal organ (VNX), but not the main olfactory bulb, impair mating behavior. Intracerebroventricular (icv)-GnRH restores mating in sexually-naïve VNX males and enhances medial amygdala (Me) activation by chemosensory stimulation. In sexually-experienced males, VNX does not impair mating and icv-GnRH suppresses Me activation. Thus, main olfactory input is sufficient for mating in experienced- but not naïve-VNX males. I tested whether GnRH enhances access of main olfactory input to the amygdala using icv-GnRH and either electrical or pharmacological stimulation of the main olfactory bulb (MOB), and then examined immediate early gene (IEG) expression there. Electrical stimulation of the MOB did not significantly activate the ipsilateral main olfactory cortex or amygdala in intact or VNX animals. When the IEG counts from both sides of the brain were averaged together, GnRH appeared to enhance activation in the medial amygdala in naïve-intact males, but appeared to decrease activation in naïve-VNX males. I concluded that electrical stimulation was not a sufficient means of driving main olfactory input to downstream brain regions, possibly due to activation of intra-bulbar inhibitory circuits. To alleviate this possible confound, I pharmacologically stimulated the MOB with a mixture of bicuculline methiodide and d,l Homocysteic acid. In sexually-naïve intact-males, MOB stimulation produced significant activation in MeAv and MePv. MePv activation is also characteristic of chemosensory stimuli from potential competitors and predators. In sexually-naïve VNX-males, in which GnRH facilitates mating, GnRH enhanced activation by MOB stimulation in posterodorsal medial amygdala (MePd), a region known to be rich in androgen resceptors and activated by conspecific reproductive chemosignals. Conversely, in sexually-experienced VNX-males, animals that do not require exogenous GnRH to mate normally after VNX, there is a depression in activation in MePd due to GnRH and stimulation in MePd, similar to its response to natural chemosensory stimulation. There also appeared to be a possible effect of VNX due to the difference in selective activation of GnRH in naïve-intact vs. naïve-VNX animals. MeP is also rich in steroid receptors and many chemosensory behaviors are steroid dependent. Therefore, I also tested the activation of androgen receptor (AR)-containing cells in Me after conspecific or heterospecific chemosensory stimulation. Conspecific and heterospecific chemosensory stimuli significantly activated AR-containing cells in Me and significantly increased the number of AR-positive cells in Me above control. The increase in the number of AR-ir cells produced by conspecific stimuli was also significantly above the numbers of AR-ir cells produced by the heterospecific stimulus. These effects may be due to increases of testosterone in response to chemosignals or circuit activity dependent on steroid levels. Future studies on castrated testosterone-replaced males will test these possibilities. The studies of this dissertation provide important information about the neurohormonal regulation of chemosensory and olfactory input to the medial amygdala. The integration of hormonal and chemosensory factors is vital to mating and other social behaviors, and thus species survival. The amygdala is crucial to this process in many vertebrate species, including the hamsters, which use chemicals to communicate with one another. This dissertation suggests, and provides some evidence for a part of the mechanism by which the amygdala accomplishes this integration.