EXCITATORY AND INHIBITORY SYNAPTIC PROCESSING IN THE ACCESSORY OLFACTORY SYSTEM OF THE FEMALE RAT

The accessory olfactory system constitutes a sensory system specifical ly involved in regulating neuroendocrine function and reproductive beh avior. The chemosensitive structure of this system, the vomeronasal or gan, exclusively innervates the accessory olfactory bulb, which in tur n projects via mono- or disynaptic pathways to a limited number of reg ions implicated in endocrine and sexual function, including the amygda la and hypothalamus. The present study investigated synaptic processin g between the different levels of this sensory system, with particular focus on the input from the accessory olfactory bulb to the medial am ygdala and the reciprocal connections between the medial amygdala and the ventromedial hypothalamus. Extracellular single-unit recordings we re obtained from medial amygdala neurons in anesthetized female rats t o study the synaptic responses elicited by stimulation of the olfactor y bulb and hypothalamus. Locally applied agonists and antagonists of a mino acid neurotransmitters were tested for their ability to mimic and block these synaptic responses in an attempt to identify the neurotra nsmitters involved in the stimulated pathways. Electrical stimulation of the accessory olfactory bulb induced orthodromic responses in 88% o f 288 medial amygdala neurons, with 67% showing orthodromic inhibition and 21% showing excitation as the shortest-latency response. Many cel ls displayed multiphasic responses with both orthodromic excitation an d inhibition. In separate experiments, main olfactory bulb stimulation also produced excitatory (39%) or inhibitory (50%) orthodromic respon ses in medial amygdala neurons (n = 105), but the latency and distribu tion of responses were significantly different than with accessory olf actory bulb stimulation. Stimulation of the ventromedial hypothalamus also had prominent excitatory (29%) or inhibitory (59%) orthodromic ac tions on the majority of amygdala neurons. Out of 288 cells tested wit h both accessory olfactory bulb and ventromedial hypothalamus stimulat ion, 79% were orthodromically responsive to both areas, whereas only 3 % responded to neither area. Fourteen (6%) medial amygdala neurons wer e antidromically activated from the ventromedial hypothalamus, and 11 of these 14 cells were simultaneously orthodromically responsive to ac cessory olfactory bulb stimulation, indicating that the accessory olfa ctory bulb can influence medial amygdala neurons that project directly to the hypothalamus. Iontophoretic application of drugs to the medial amygdala revealed that glutamate and GABA consistently mimicked the o rthodromic excitatory and inhibitory responses, respectively, from bot h the accessory olfactory bulb and ventromedial hypothalamus. In some cases, ejection of bicuculline could block or reverse excitation of th e orthodromic inhibitory responses, whereas kynurenic acid could elimi nate the orthodromic excitation, indicating that excitatory and inhibi tory amino acid transmitters are at least partially involved in these pathways. These findings form a framework for determining the synaptic mechanisms underlying information processing in the accessory olfacto ry system and olfactory modulation of reproductive function.