Neural Mechanisms of Courtship and Memory in Drosophila
Research in the Siwicki lab focuses on understanding the neurobiology of courtship behavior and memory in the fruit fly, Drosophila melanogaster. The behavioral responses of wild-type male fruit flies to the aphrodisiac properties of female flies are largely instinctive - males reared in social isolation actively court virgin females. But male flies often encounter sexually attractive individuals that are not receptive to mating, e.g., immature virgin females, or mature females that recently mated with another male. In fact, males can learn from their attempts to court unreceptive targets, and the neural processes responsible for this learning are the focus of our interests. Specifically, we aim to identify the neural circuits and mechanisms of synaptic plasticity responsible for a form of associative learning known as courtship conditioning. In this learning paradigm, after males are paired with an unreceptive, previously mated female for an hour, they suppress their courtship of other females for 1-2 hours (Seigel and Hall, 1979).
Several years ago we evaluated the role of the mushroom bodies (MB) in courtship conditioning by pharmacologically ablating the MBs in early larval development. Our results indicated that the MBs are not required for innate male courtship behavior, but are required for normal memory of courtship conditioning (McBride et al. 1999). MB-ablated males showed only a transient memory of conditioning; their courtship behavior returned to naïve levels within 30 minutes after training. Similar results were obtained in more recent studies in our lab, involving GAL4/UAS manipulations of MB function. The evidence suggests that memory assayed immediately after training (0 minutes) is independent of MB function, while memory lasting 30 minutes or longer requires MB processing.
We also described two novel training protocols that produced long-term memory of courtship conditioning (McBride et al., 1999). One consists of a continuous 5-h pairing with a mated female. The other consists of 3 sets of 1-h pairings, interrupted by 30-60 min breaks. For up to 8 days after these intensive training regimes, males showed a significant suppression of courtship activity relative to age-matched naïve controls. Other researchers have adopted our training procedures to assess the roles of other genes in long-term memory (Presente et al., 2004; Sakai et al., 2004). Meanwhile, students in our lab continue to investigate additional training paradigms for inducing both short-term and long-term courtship memory.
In spite of the likely ecological relevance of courtship conditioning, progress in deciphering its neural mechanisms has been impeded by its complexity, specifically by the multisensory nature of the training experience with mated females. We have begun to define the relevant sensory cues in collaboration with Jean-Francois Ferveur and coworkers at the Universite de Bourgogne in Dijon, France. Using flies of different genotypes that express distinct cuticular hydrocarbon blends (Ferveur et al., 1997), we have identified a specific role for female cuticular pheromones as a conditioned stimulus in courtship conditioning. With current molecular and genetic tools for identifying the sensory neural systems that transduce sex pheromones (Bray and Amrein, 2003), these studies will contribute to understanding the behavioral significance of different components of the pheromonal blend in innate vs. learned aspects of courtship behavior.
Bray, S. and Amrein, H. 2003. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019-1029.
McBride, S.M.J., Giuliani, G., Choi, C., Krause, P., Correale, D., Watson, K., Baker, G. and Siwicki, K.K. 1999. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster Neuron 24: 967-977.
Presente, A., R.S. Boyles, C.N. Serway, S.J. deBelle, A.J. Andres, 2004, Notch is required for long-term memory in Drosophila, Proc. Natl. Acad. Sci. USA 101:1764-1768
Sakai, T., T. Tamura, T. Kitamoto, and Y. Kidokoro, 2004, A clock gene, period, plays a key role in long-term memory formation in Drosophila. Proc. Natl. Acad. Sci. USA 101: 16058 -16063
Siegel, R.W. and Hall, J.C. 1979. Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 76: 3430-3434.
Tompkins, L., Siegel, R.W., Gailey, D.A. and Hall, J.C. 1983. Conditioned courtship in Drosophila and its mediation by association of chemical cues. Behav. Genet. 13: 565-578.
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Siwicki, K.K. and C.A. Bishop, 1986, Mapping of proctolin-like immunoreactivity in the nervous systems of lobster and crayfish. J. Comp. Neurol. 243: 435-453
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Dockendorff, T.C., H.S. Su, S.M.J. McBride, Z. Yang, C. Choi, K.K. Siwicki, A. Sehgal, and T.A. Jongens, 2002, Drosophila lacking dfmr1 activity show defects in circadian output and fail tomaintain courtship interest. Neuron 34: 973-984
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Mc Bride, S.M.J., C.H. Choi, Y. Wang, D. Liebelt, E. Braunstein, D. Ferrero, A. Sehgal, K.K. Siwicki, T.C. Dockendorff, H.T. Nguyen, T.V. McDonald and T.A. Jongens, 2005, Pharmacological rescue of synaptic plasticity, courtship behavior and mushroom body defects in a Drosophila model of Fragile X Syndrome. Neuron 45: 753-764
Siwicki, K.K., P. Riccio*, L. Ladewski*, F. Marcillac, L. Dartevelle, S.A.
Cross* and J.-F. Ferveur, 2005, The role of cuticular pheromones in
courtship conditioning of Drosophila males, Learning & Memory 12: 636-645