Neurotransmitter release in the accessory olfactory bulb during and after the formation of an olfactory memory in mice.

Female mice form an olfactory memory to the pheromones of the mating male during a critical period after mating. Previous experiments have shown that the neural changes underlying this memory are located in the accessory olfactory bulb, are dependent on noradrenergic neurotransmission, and most likely involve changes at the mitral-granule cell reciprocal synapses. Using the technique of in vivo microdialysis we have followed changes in a range of neurotransmitters before, during and after memory formation. The increase in GABA levels in response to a glutamate challenge was greater during and after memory formation than before. The aspartate/GABA ratio was decreased following memory formation, during exposure to the pheromones of the mating male. These findings are consistent with our hypothesis that memory formation involves a long-lasting increase in the inhibition of the subset of mitral cells that respond to the mating male's pheromones. Unexpectedly, there were increases in the concentrations of the excitatory transmitters glutamate and aspartate in non-mating females, immediately following male exposure, and two days later in response to re-exposure to the same male pheromones. These results suggest that exposure to male pheromones alone, without the association of mating, causes a long-lasting decrease in the inhibitory control of the subset of mitral cells responding to these pheromones. The implication of these results is that two types of synaptic plasticity can occur in the accessory olfactory bulb. The association of mating and pheromonal exposure induces memory formation by increasing the inhibition of the pheromonal signal at the level of the accessory olfactory bulb, thereby preventing them from activating the neuroendocrine block to pregnancy. Male exposure without mating appears to have the opposite effect, decreasing the inhibition of the pheromonal signal and potentiating the oestrous-inducing effects of the male pheromones.