Synaptic Mechanisms of Olfactory Recognition Memory

Abstract

The complexity and inaccessibility of the mammalian brain prevent the localization and description of memory traces and the definition of the processes that produce memories. The model reviewed here is the olfactory recognition memory formed to male pheromones by a female mouse at mating. The memory trace has been localized to the reciprocal dendrodendritic synapse between mitral cells and granule cells in the accessory olfactory bulb. An increase in noradrenaline after mating reduces inhibitory transmission of gamma-aminobutyric acid (GABA) from the granule cells to mitral cells and induces an olfactory memory of pheromones present at mating. Recent work has shown that the activation of mGluR2, a metabotropic glutamate receptor, localized at granule cell dendrites suppresses the GABA inhibition of the mitral cells and permits the formation of a specific olfactory memory that faithfully reflects the memory formed at mating. This simple olfactory memory may provide an excellent model system with which to investigate the molecular mechanisms of the synaptic plasticity involved in learning and memory.

Synaptic Mechanisms Underlying Pheromonal Memory in Vomeronasal System

“…The process of pregnancy is not disturbed by the pheromones of a partner male. Thus, the Bruce effect was thought to be a very useful model to study the pheromone-induced olfactory memory (pheromonal memory) (Brennan et al , 1990, Kaba andNakanishi 1995). On the other hand, the vomeronasal system has an important role in the processing of pheromonal information (Halpern, 1987).…”

“…2). Pheromonal information is transmitted via the AOB and the amygdaloid nucleus to the hypothalamus, and disturbs the reproductive neuroendocrine function that is necessary for the maintenance of pregnancy (Keverne, 1983;Kaba and Nakanishi, 1995;Brennan and Keverne, 1997;Brennan, 2001;Keverne, 2002). Our research objective was to analyze the synapse mechanisms in the vomeronasal system underlying pheromonal memory.…”

“…(1) Memory formation depends on vaginocervical stimulation at mating, but requires a prolonged exposure of 4 to 6 hr to male pheromones immediately after mating (Keverne, 1983;Kaba and Nakanishi, 1995). Exposure to male pheromones alone is insufficient to produce a memory.…”

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

“…The elevation of Ca 2ϩ might be critical for plastic changes at the dendrodendritic synapses in the main OB. Because the formation of olfactory and pheromonal memories involves long-lasting plastic changes at dendrodendritic reciprocal synapses in the main and accessory OBs, respectively (Kaba and Nakanishi, 1995;Brennan and Keverne, 1997), the enhanced granule-to-mitral inhibition might be relevant to the long-lasting plasticity of dendrodendritic synapses associated with olfactory memory during slowwave sleep. Odor learning induces a substantial increase in inhibitory neurotransmission (Wilson et al, 1987;Brennan and Keverne, 1997).…”

α2-Adrenergic receptor activation promotes long-term potentiation at excitatory synapses in the mouse accessory olfactory bulb

“…This mate recognition memory is essential for preventing the activation of the neuroendocrine mechanisms leading to pregnancy loss (Keverne and Rosser 1986). It has been hypothesized that the mate recognition memory functions as a gate to suppress or modulate the mate's chemosignals at the level of the AOB (Brennan et al 1990;Kaba and Nakanishi 1995;Brennan and Zufall 2006;Griffiths and Brennan 2015). Synaptic connections in the external plexiform layer (EPL) of the AOB are dominated by the reciprocal dendrodendritic synapses between MCs, a single class of projection neurons, and granule cell (GC) interneurons.…”