Long-term enhancement of synaptic transmission between antennal lobe and mushroom body in cultured Drosophila brain

In Drosophila, the mushroom body (MB) is a critical brain structure for olfactory associative learning. During aversive conditioning, the MBs are thought to associate odour signals, conveyed by projection neurons (PNs) from the antennal lobe (AL), with shock signals conveyed through ascending fibres of the ventral nerve cord (AFV). Although synaptic transmission between AL and MB might play a crucial role for olfactory associative learning, its physiological properties have not been examined directly. Using a cultured Drosophila brain expressing a Ca2+ indicator in the MBs, we investigated synaptic transmission and plasticity at the ALMB synapse. Following stimulation with a glass micro-electrode, AL-induced Ca2+ responses in the MBs were mediated through Drosophila nicotinic acetylcholine receptors (dnAChRs), while AFV-induced Ca2+ responses were mediated through Drosophila NMDA receptors (dNRs). ALMB synaptic transmission was enhanced more than 2 h after the simultaneous associative-stimulation of AL and AFV, and such long-term enhancement (LTE) was specifically formed at the ALMB synapses but not at the AFVMB synapses. ALMB LTE was not induced by intense stimulation of the AL alone, and the LTE decays within 60 min after subsequent repetitive AL stimulation. These phenotypes of associativity, input specificity and persistence of ALMB LTE are highly reminiscent of olfactory memory. Furthermore, similar to olfactory aversive memory, ALMB LTE formation required activation of the Drosophila D1 dopamine receptor, DopR, along with dnAChR and dNR during associative stimulations. These physiological and genetic analogies indicate that ALMB LTE might be a relevant cellular model for olfactory memory.