Abstract
Electrical synapses between neurons, also known as gap junctions, are direct cell membrane channels between adjacent neurons. Gap junctions play a role in the synchronization of neuronal network activity; however, their involvement in cognition has not been well characterized. Three-hour olfactory associative memory in Drosophila has two components: consolidated anesthesia-resistant memory (ARM) and labile anesthesia-sensitive memory (ASM). Here, we show that knockdown of the gap junction gene innexin5 (inx5) in mushroom body (MB) neurons disrupted ARM, while leaving ASM intact. Whole-mount brain immunohistochemistry indicated that INX5 protein was preferentially expressed in the somas, calyxes, and lobes regions of the MB neurons. Adult-stage-specific knockdown of inx5 in αβ neurons disrupted ARM, suggesting a specific requirement of INX5 in αβ neurons for ARM formation. Hyperpolarization of αβ neurons during memory retrieval by expressing an engineered halorhodopsin (eNpHR) also disrupted ARM. Administration of the gap junction blocker carbenoxolone (CBX) reduced the proportion of odor responsive αβ neurons to the training odor 3 hours after training. Finally, the α-branch-specific 3-hour ARM-specific memory trace was also diminished with CBX treatment and in inx5 knockdown flies. Altogether, our results suggest INX5 gap junction channels in αβ neurons for ARM retrieval and also provide a more detailed neuronal mechanism for consolidated memory in Drosophila.
Highlights
IntroductionPavlovian olfactory learning in Drosophila melanogaster, the fruit fly, is a well-characterized behavioral paradigm in which flies are subjected to a training session of sequential exposures to two distinct odors (conditioned stimulus, CS) with or without electric foot shock (unconditioned stimulus, US)[1]
Pavlovian olfactory learning in Drosophila melanogaster, the fruit fly, is a well-characterized behavioral paradigm in which flies are subjected to a training session of sequential exposures to two distinct odors with or without electric foot shock[1]
Electrical synapses between mushroom body are critical for consolidated memory retrieval in Drosophila
Summary
Pavlovian olfactory learning in Drosophila melanogaster, the fruit fly, is a well-characterized behavioral paradigm in which flies are subjected to a training session of sequential exposures to two distinct odors (conditioned stimulus, CS) with or without electric foot shock (unconditioned stimulus, US)[1]. Electrical synaptic transmission depends on clusters of intercellular channels called gap junctions, which form the pores approximately 1.2 nm in diameter between neurons[6]. These pore structures allow diffusion of small molecules and ions, enabling bidirectional electronic signal transmission between neurons. Our previous study showed that two MB modulatory neurons in the Drosophila brain, the anterior paired lateral (APL) and dorsal paired medial (DPM) neurons, formed heterotypic gap junction channels via INX6 and INX7, and that disrupting communication through these gap junctions impaired 3-hour ASM[12]. A recent study indicated that gap junctions in αβ, α'β', and MB output neurons (MBON-β'2mp) were involved in Drosophila visual learning[13]
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