The control of song pattern generation in Drosophila: Circuit mechanisms and sensory modulation
Final Report Abstract
How does coordinated neuronal activity in the brain produce complex behaviors, and how can the brain rapidly adjust its behavioral output to incoming sensory information? While it is easy to ask these questions about the human brain, it is challenging to find answers, given the huge number of neurons and connections in the human brain. In my project I hence asked the same questions, about the comparatively small brain of the fruit fly, Drosophila melanogaster. When flies try to find a suitable mating partner, they exhibit a complex courtship ritual, during which the male attempts to convince the female to mate. While he chases the female, he sings to her by vibrating a single wing. She, in turn, listens to his song, evaluates song quality and provides sensory feedback to the male by running away or slowing down. Then the male uses this feedback to update his song, repeating this back and forth until the female ultimately accepts or rejects the male. How does coordinated neuronal activity in the brain of the male fly produce his complex song behavior? Out of the hundreds of thousands of neurons in the fly’s nervous system, only on the order of tens of neurons are currently thought to contribute to the male’s song behavior. While we know the identity of these neurons in the male song circuit, we lack a clear understanding of how these neurons interact during song, and how patterned activity of individual neurons shapes song dynamics. I exploited the genetic toolkit available in Drosophila to map the “song repertoire” of each individual type of song neuron, which allowed me to form hypotheses on how these neurons might interact during song production. I went on to test these hypotheses using sophisticated neural imaging methods. I found evidence for a neural circuit motif that allows the male to switch between different song modes (termed “sine” and “pulse” song), using a combination of mutual inhibition and “post-inhibitory rebound” (that is, neural activity induced by release from inhibition). These results improve our understanding of the neural circuitry underlying complex song behavior of the fly. Can the male fly learn new courtship behavior in a novel sensory context? The courtship behavior of the male fly is innate, meaning a male that has never seen other flies before can perform his complex courtship ritual the first time he meets a female. Innate behaviors are genetically hard-wired and therefore often assumed to be inflexible, not amenable to learning. Yet, previous work has shown that male flies can learn to suppress their courtship drive after exposure to unreceptive females. Based on this finding, I asked whether male flies can learn to adjust their song behavior (without suppressing it) to a new sensory context. Specifically, I tested whether males change their innate song behavior when they experience a female that walks backwards (a behavior females do not usually show) every time he sings a particular type of song (“pulse” song). Notably, I found that males indeed change their song behavior compared to controls, and even maintain the changed behavior when paired with a “normally” behaving female: males learn to sing more directly behind the female (as opposed to a broad range of angles around the female during natural courtship). This is particularly surprising because the learned behavior seems optimized to the new sensory context: The only way to be closer to a backward-walking female after singing than before is to sing straight behind her, which is what the male seems to learn.
Publications
- (2018). Discovery of a new song mode in Drosophila reveals hidden structure in the sensory and neural drivers of behavior. Current Biology, 28(15), 2400-2412
Clemens, J., Coen, P., Roemschied, F. A., Pereira, T. D., Mazumder, D., Aldarondo, D. E., & Murthy, M.
(See online at https://doi.org/10.1016/j.cub.2018.06.011) - (2019). An inhibitory circuit motif within the brain underlies song patterning decisions in Drosophila melanogaster. CSHL Neurobiology of Drosophila meeting, Cold Spring Harbor
Roemschied FA, Pacheco Pinedo D, Murthy M
- (2019). Modification of Drosophila courtship songs via closed-loop perturbation of sensory feedback. Gordon Research Conference on Neuroethology, Mt. Snow
Roemschied FA, Calhoun AJ, Ireland EC, Choi MS, Murthy M
- (2020). Probing song motor circuit architecture and function in Drosophila melanogaster. Cosyne, Denver
Roemschied FA, Pacheco Pinedo D, Li X, Ireland EC, Murthy M
- Flexible circuit mechanisms for context-dependent song sequencing. Nature (2023).
Frederic A. Roemschied, Diego A. Pacheco, Elise C. Ireland, Xinping Li, Kyle Thieringer, Max J. Aragon, Rich Pang, Mala Murthy
(See online at https://doi.org/10.1038/s41586-023-06632-1)
