Neural basis of flexible courtship behavior

• Applicant: Dr. Madhura Ketkar
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: since 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 550900910

Persistent motivational states allow animals to engage in prolonged activities until their expected goal is achieved. For example, courtship drive in various species must persist for several minutes or even hours until their courtship ritual convinces a conspecific of mating. However, not every courtship attempt culminates in mating, and mechanisms to assess the mating likelihood should be in place to minimize the costs towards fruitless courtship. On the one hand, cues from conspecifics indicate their likelihood of mating, and the chance to court a high-likelihood conspecific should be exploited by being more persistent. On the other hand, long futile courtship of any conspecific can be viewed as sunk costs and should be discontinued in favor of an exploratory behavioral switch. How is such ‘explore-vs-exploit’ trade-off settled in social behaviors? Here, I propose to examine the neural mechanisms behind this trade-off in the courtship of fruit flies, Drosophila melanogaster. Male fruit flies engage in enduring pursuit of females for several minutes, while adopting a progressively explorative courting strategy if no mating occurs (preliminary results). Whereas the key Drosophila neurons underlying the persistent courtship drive have been described, how the persistence subsides over time in the absence of mating is unknown. I will combine fly behavior and in vivo neuronal imaging with genetic interventions to reveal the determinants of the explore-vs-exploit courting strategy in flies and how they interact within the male’s brain. In particular, by optogenetically evoking female acceptance or rejection cues, I will determine if the courting male uses distinct female behaviors as evidence of waxing or waning of the mating likelihood. Conversely, removing the female feedback cues will reveal if male-intrinsic mechanisms track the time spent courting and change the courting strategy autonomously. To understand how the brain encodes these evidences of mating likelihood, I will characterize individual neurons in the male courtship circuit. Courtship command neurons P1 integrate sensory and internal state-related information, and regulate the males’ courtship engagement. I hypothesize that the female feedback alters P1 excitability, through dopaminergic, serotonergic or octopaminergic neuromodulation representing the innate valence of the feedback. I further propose that the temporal dynamics of the sustained pCd neurons might function as an innate time-tracking mechanism downstream of P1. Lastly, I will develop a data-driven model to explain how the female cues and the male brain co-regulate the male’s courtship strategy. Altogether, these approaches will reveal the neural correlates and the computation underlying adaptability in persistent courtship. While uncovering the neural principles of an explore-vs-exploit decision, this project will elucidate how the brain incorporates fluctuating estimates of expected outcome into persistent internal states.

• DFG Programme: WBP Position