Abstract
The secrets of memory have tantalized people for centuries. Excitingly neuroscientists using fly Drosophila melanogaster as the model animal to study memory started to manipulate different forms of memory at different processing stages from genes or molecules to circuits. As more and more evidence accumulate a picture addressing how the memory is formed in the fly brain is getting complete. This dissertation reveals two additional roles of the anterior paired lateral (APL) neuron in the intermediate-term memory (ITM), in addition to the known role in olfactory learning. Gap junctions, or electrical synapses, are important for normal brain functions but their contribution to memory formation has not been well characterized. We have shown that two extrinsic neurons, the APL and DPM neurons, form gap-junctional communication in the mushroom body (MB), the learning and memory center in the fly brain. Fly olfactory associative conditioning produces two components of ITM: anesthesia-sensitive memory (ASM) and anesthesia-resistant memory (ARM). Following disruption with RNAi-mediated knockdowns of inx7 and inx6 in the APL and DPM neurons, respectively, we found that flies showed normal olfactory associative learning and intact ARM but could not form 3-h ASM. These data reveal that the heterotypic gap junctions between the APL and DPM neurons are an essential part of the MB circuitry for ASM, suggesting that a recurrent neural circuit, consisting of APL, DPM and MB neurons, may stabilize ASM within the MB. In addition to the gap-junctional role of the APL and DPM neurons in ASM, we also have shown that the chemical neurotransmission from the APL neurons, after conditioning but before testing, is necessary for ARM formation. Immunostaining and an adult-stage-specific RNAi knockdown indicated that octopamine from the APL neuron acts on MB α′β′ Kenyon cells (KCs) via Octβ2R octopamine receptors to modulate ARM formation. Surprisingly the serotoninergic DPM—αβ KCs pathway and the octopaminergic APL—α′β′ KCs pathway are additive for 3-h ARM, suggesting they modulate ARM formation in the MB in parallel.