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Influence of Hormonal State on Behavioral Plasticity in the Fruit Fly Drosophila melanogaster


Developing insects shed old cuticle at the end of each stage by performing a sequence of patterned muscle contractions, a process referred to as ecdysis. This behavioral sequence is initiated by endocrine peptides called “ecdysis triggering hormone” (ETH). Although ETH signaling components persist in the adult fruit fly Drosophila melanogaster, their function(s) during adulthood have not been studied.

To elucidate functions of ETH signaling in adult behavior, I investigated possible roles of ETH-driven hormonal state in learning and memory processes of male Drosophila by using a simple social learning paradigm, courtship conditioning. First, I show that ETH regulates short-term memory performance of males recently rejected by mated females. Adult ETH signaling regulates memory retention through maintenance of juvenile hormone (JH) production. The requirement of JH for normal memory performance is confined to a critical period during the first three days of adult life. JH targets dopaminergic neurons to maintain the short-term courtship memory (STM).

Next, I show that ETH signaling also modulates long-term memory (LTM) formation through pathways distinct from those regulating STM. ETH is necessary and sufficient to induce memory formation through de novo protein synthesis. RNAi knockdown experiments reveal that ETH signaling regulates LTM through both direct and JH synthesis-mediated indirect modulation of memory circuits. As described for emotional memory circuits in the limbic system of mammals, actions of ETH and JH converge mainly in specific mushroom body neuropils to regulate LTM. Since ETH induces calcium mobilization in memory circuit neurons, I propose that the essential nature of hormonal state in regulation of memory circuits involves calcium-dependent mechanisms.

Although ETH promotes calcium mobilization in target cells, the intracellular signal transduction machinery induced by ETH receptors is largely based on logical inference. To investigate the specific steps in ETH receptor (ETHR)-induced signaling within target neurons, I used the pupal ecdysis sequence of Drosophila as a bioassay system. I identified a series of putative downstream G protein-coupled receptor (GPCR) signaling steps in pupal ETHR-expressing bursicon neurons. I also show that ETH-driven internal calcium mobilization is dependent on calcium influx from the extracellular space, possibly by promoting TRP channel activities, which provides a new link between the ETHR-driven intracellular cascade and membrane channels important for induction of electrical activity in target neurons.

Lastly, I describe that neurons expressing the neuropeptide crustacean cardioactive peptide (CCAP) have different functions in adult male and female Drosophila. In males, activity of CCAP neurons is important in gender recognition. Chemical signaling from CCAP neurons is required for suppression of abdominal contractions during the courting. In females, CCAP neurons are important for oviposition. In particular, regulate oviposition and choice of oviposition site. This finding contributes new insight into neuropeptide-based sexual dimorphic behaviors.

In summary, my dissertation work reveals functions for circulating peptides acting on the CNS to regulate behavioral plasticity of Drosophila.

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