Mating proximity blinds threat perception

[sl8]

https://www.nature.com/articles/s41586-024-07890-3

Article
Open access
Published: 28 August 2024

Mating proximity blinds threat perception

Laurie Cazalé-Debat, Lisa Scheunemann, Megan Day, Tania Fernandez-d.V. Alquicira, Anna Dimtsi, Youchong Zhang, Lauren A. Blackburn, Charles Ballardini, Katie Greenin-Whitehead, Eric Reynolds, Andrew C. Lin, David Owald & Carolina Rezaval

Nature (2024)

Abstract

Romantic engagement can bias sensory perception. This ‘love blindness’ reflects a common behavioural principle across organisms: favouring pursuit of a coveted reward over potential risks1. In the case of animal courtship, such sensory biases may support reproductive success but can also expose individuals to danger, such as predation2,3. However, how neural networks balance the trade-off between risk and reward is unknown. Here we discover a dopamine-governed filter mechanism in male Drosophila that reduces threat perception as courtship progresses. We show that during early courtship stages, threat-activated visual neurons inhibit central courtship nodes via specific serotonergic neurons. This serotonergic inhibition prompts flies to abort courtship when they see imminent danger. However, as flies advance in the courtship process, the dopaminergic filter system reduces visual threat responses, shifting the balance from survival to mating. By recording neural activity from males as they approach mating, we demonstrate that progress in courtship is registered as dopaminergic activity levels ramping up. This dopamine signalling inhibits the visual threat detection pathway via Dop2R receptors, allowing male flies to focus on courtship when they are close to copulation. Thus, dopamine signalling biases sensory perception based on perceived goal proximity, to prioritize between competing behaviours.

Main

Every day animals make decisions that require balancing opportunities and risks. This trade-off has been explored in humans4,5, rodents6,7 and invertebrates8,9,10,11,12,13,14. However, we still lack a detailed mechanistic understanding of how conflict is resolved in the brain, particularly when the dangers and benefits are crucial life choices.

One especially important trade-off is between survival and reproduction. Avoiding threats can be a life-saving decision, but excessive caution might result in missed mating opportunities. Recent work has revealed how sex drive and threat avoidance are independently signalled in the brain15,16,17,18,19,20,21, yet it remains unclear how these needs are prioritized when they are in conflict. How animals suppress courtship when it is better to run away, and how this is reversed when the rewards of courtship outweigh the risk of predation (for example, if mating is imminent) still remain unknown.

Dopamine is a key player in motivation, need and reward22,23,24. Beyond these functions, dopamine is thought to relay the value of sensory input and internal/behavioural states to decision-making centres, thus adapting behaviour23,25,26. Yet, how dopamine dynamically modulates sensory valence and influences decision-making during conflict remains poorly understood. This task could be mediated through sensory filter systems27, which block superfluous inputs and highlight relevant information to facilitate appropriate behaviours. Such filtering systems could thus serve as a means to shut down competing sensory inputs when animals are close to achieving a crucial goal. Here we describe a state-dependent filter system driven by dopamine that allows Drosophila males to filter out external threats and focus on courtship when they are close to mating.

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[hunter]

1. My first courtship nearly killed me, that's for sure...