A new memory specific adenylyl cyclase in Drosophila olfactory memory

Ajuria, L. 1 , Musso, P. 1 , Gervasi, N. 2 , Tchenio, P. 1, 3 & Preat, T. 1

1 Genes and Dynamics of Memory Systems, Neurobiology Unit, CNRS, Ecole Supérieure de Physique et de Chimie Industrielles, Paris, France
2 Inserm, UMR-S 839, Institut du Fer à Moulin, Paris, France
3 Biophotonique, Université Paris-Sud, CNRS UPR 3321, Orsay, France.

The cAMP/PKA pathway is a critical pathway in memory formation from invertebrate to vertebrate systems. In Drosophila, the cAMP pathway is activated in the mushroom body (MB) during olfactory memory formation, in which an odor is paired with electric shock punishment that leads to a learnt avoidance of the associated odor. The MB is the main associative learning and memory center in insects and in Drosophila it is composed of three main subpopulation of neurons: ??, ? and ????. The distinct morphologies and expression profiles of each subpopulation suggests that they play different roles in memory formation.
In the MB, G-protein-coupled receptors (GPCR) are activated by the unconditioned stimulus (shock), during the classical olfactory conditioning, which activates an adenylyl cyclase (AC) leading to the increase of cAMP second messenger. This effect is potentiated by the synergistic activation of the AC by Ca2+/CaAM through the conditioned stimulus pathway (odor). The cAMP then activates its downstream target PKA leading to memory formation.
One of the first described gene involved in Drosophila olfactory learning, rutabaga, encodes for an AC. Rutabaga is the responsible of the coincidence detection of odor and shock information in ?? and ? neurons but it has been shown to be dispensable in the ???? neurons. This suggests that there could be another AC playing the role of a coincidence detector in the prime neurons.
So far, by bath application of dopamine and acetylcholine in in vivo brain imaging, we have found an AC that contributes to coincidence detection in prime neurons. The reduction of PKA activity observed in imaging experiments correlates with a specific behavioral memory deficit. These results suggest that more than one AC could be involved in olfactory memory in Drosophila, possibly in a memory specific manner.