Otopalik, A. | bioRxiv Science

bioRxiv2024

Social state gates vision using three circuit mechanisms in Drosophila

Animals are often bombarded with visual information and must prioritize specific visual features based on their current needs. The neuronal circuits that detect and relay visual features have been well-studied. Yet, much less is known about how an animal adjusts its visual attention as its goals or environmental conditions change. During social behaviors, flies need to focus on nearby flies. Here, we study how the flow of visual information is altered when female Drosophila enter an aggressive state. From the connectome, we identified three state-dependent circuit motifs poised to selectively amplify the response of an aggressive female to fly-sized visual objects: convergence of excitatory inputs from neurons conveying select visual features and internal state; dendritic disinhibition of select visual feature detectors; and a switch that toggles between two visual feature detectors. Using cell-type-specific genetic tools, together with behavioral and neurophysiological analyses, we show that each of these circuit motifs function during female aggression. We reveal that features of this same switch operate in males during courtship pursuit, suggesting that disparate social behaviors may share circuit mechanisms. Our work provides a compelling example of using the connectome to infer circuit mechanisms that underlie dynamic processing of sensory signals.

neuroscience↗

bioRxiv2020

An arousal gated visual circuit controls pursuit during Drosophila courtship

Long-lasting internal states, like hunger, aggression, and sexual arousal, pattern ongoing behavior by defining how the sensory world is translated to specific actions that subserve the needs of an animal. Yet how enduring internal states shape sensory processing or behavior has remained unclear. In Drosophila, male flies will perform a lengthy and elaborate courtship ritual, triggered by activation of sexually-dimorphic P1 neurons, in which they faithfully follow and sing to a female. Here, by recording from males as they actively court a fictive female in a virtual environment, we gain insight into how the salience of female visual cues is transformed by a males internal arousal state to give rise to persistent courtship pursuit. We reveal that the gain of LCt0a visual projection neurons is strongly increased during courtship, enhancing their sensitivity to moving targets. A simple network model based on the LCt0a circuit accurately predicts a males tracking of a female over hundreds of seconds, underscoring that LCt0a visual signals, once released by P1-mediated arousal, become coupled to motor pathways to deterministically control his visual pursuit. Furthermore, we find that P1 neuron activity correlates with fluctuations in the intensity of a males pursuit, and that their acute activation is sufficient to boost the gain of the LCt0 pathways. Together, these results reveal how alterations in a males internal arousal state can dynamically modulate the propagation of visual signals through a high-fidelity visuomotor circuit to guide his moment-to-moment performance of courtship.

neuroscience↗