世人已被記憶的神祕面紗迷惑了好幾世紀。令人振奮地，現今以果蠅作為模式生物來研究記憶的神經科學家，已經可以從分子、基因、甚至是神經迴路的層級，在不同的時間點操縱各種不同型式的記憶。隨著愈來愈多的研究證據發表，我們漸漸能夠描繪出一個完整的劇本來說明記憶如何在果蠅的大腦中形成？這篇論文揭露一顆原本就知道參與嗅覺學習的APL神經元，還有另外兩種幫助中期記憶形成的功能。間隙連接，或者說電突觸，在腦中扮演重要的角色。但是它們如何參與記憶形成的機制則尚未被研究。我們已經證明果蠅腦中學習與記憶的中樞(蕈狀體)的兩種外源神經元(APL神經元及DPM神經元)間，存在著間隙連接。果蠅的嗅覺關聯性制約可以產生兩種不同的中期記憶—昏迷敏感性記憶和抗昏迷記憶。利用核糖核酸干擾術來降低inx6和inx7，各自在DPM神經元和APL神經元的表現量之後，我們觀察到果蠅的學習能力和三小時抗昏迷記憶都是正常，但無法形成三小時昏迷敏感性記憶。這些觀測數據證明APL神經元和DPM神經元所組成的異質間隙連接，是蕈狀體迴路在形成昏迷敏感性記憶時，一個重要的元件。也暗示一個由APL神經元、DPM神經元和肯氏細胞組成的復發性神經迴路，在蕈狀體中負責穩固昏迷敏感性記憶。除了APL神經元與DPM神經元形成的間隙連接參與了昏迷敏感性記憶外，我們還發現抗昏迷記憶在固化的時期，須要APL神經元的化學神經傳輸。透過免疫染色和成蟲專一的核糖核酸干擾技術，我們確立這個神經機制—APL神經元釋放出羥苯乙醇胺(octopamine)，活化表現在α′β′肯氏細胞上的Octβ2R，進而調控抗昏迷記憶的形成。令人驚訝地，2011年的研究報告中提及的發現—DPM神經元所釋放的血清素會活化αβ肯氏細胞，同樣地調控抗昏迷記憶的形成。在同一隻果蠅操縱這兩種神經機制，我們看到加成的效果，暗示它們在蕈狀體中平行獨立地運作。

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.

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