Integrating visual information with an internal sexual arousal state

Animals must navigate complex visual environments, ensuring they avoid dangers while also foraging for food or finding a mate. To succeed, animals must identify relevant visual cues and interpret them in relation to their external circumstances and internal state, ensuring they respond appropriately. Visual information is perceived non-discriminately in the eye; however, how the animal responds to this information is determined in the brain. Understanding how the brain transforms complex visual stimuli into complex behaviour patterns remains a significant challenge in behavioural neuroscience. The elegant courtship display of the male vinegar fly Drosophila melanogaster is ideally suited to address this challenge. To reproduce successfully, Drosophila males are hardwired, having the ability to navigate complex environments and identify a mate. The interpretation of the female as a potential mate triggers a behavioural switch in males, setting off an elaborate behavioural display: males persistently pursue the female while intermittently singing her a courtship song through the extension and vibration of a single wing. Meanwhile, the female continuously decamps and rejects the male's advances, giving her time to assess his suitability as a mate before she sanctions the mating. This switch in the males' behavioural pattern is triggered when a sexual arousal threshold is reached, a stable internal state ensuring males persist in pursuing the female. Interestingly, this behavioural switch must also be flexible. If males, once aroused, find the female is, in fact, a different species or sex, they must switch back to their pre-arousal behavioural patterns.

Studies in the vinegar fly Drosophila melanogaster can provide insights into general principles of how brains use sensory information, like visual stimuli, to guide behaviour and how internal state changes, such as arousal, modify these sensorimotor programs. Working with flies has the advantage of using a vast array of genetic tools that allows us to identify and manipulate relevant neurons in the brain. Using these tools, we will study a group of sexually-dimorphic neurons involved in visual integration critical to male courtship behaviour and reproductive success.This proposal will be an ideal entry point into our understanding of how animals integrate external sensory information with their internal state to make an appropriate context-dependent decision.

Visual stimuli must be interpreted within a complex and ever-changing environment to instruct appropriate behavioural responses. A moving object, for example, could be a potential mate, a competitor, a predator, or an irrelevant object. Each of these possibilities requires the initiation of different sensory-motor transformations. In a species with a well-developed visual system, the animal's response may depend on the presence or absence of specific visual cues, their temporal and spatial relationships, their context and the animal's arousal state.

We aim to elucidate the mechanisms by which higher-order processing centres in the brain integrate visual and state-dependent information to confer meaning to visual signals in the context of reproductive behaviours. Upon identifying a suitable partner, Drosophila melanogaster males initiate an elaborate courtship ritual that culminates with copulation. We hypothesise that in the fly, sex-specific neural circuitry in the central brain integrates visual information with an internal state of sexual arousal, activating motor programmes for initiating, controlling, and fine-tuning visually guided courtship behaviours. We have identified a candidate sexually dimorphic central brain neural cluster that likely mediates arousal-dependent visual processing in males. This study will define the role of these neurons in visually guided male courtship behaviour, establishing their connectivity with visual and motor pathways and the mechanism underlying the 'state-switch' to arousal and sexual activity.