Starvation modulates associative short-term memory of Drosophila in a task-dependent manner

It is widely believed that starvation favours the processing of food-related cues, a notion here called the adaptive specificity hypothesis. Indeed, in Drosophila melanogaster starvation is required for appetitive odour-sugar but not for aversive odour-shock memory. Results from Gruber et al. (2013) and Meschi et al. (2024), however, suggest that starvation improves aversive short-term memory, too, challenging this hypothesis. We survey how starvation affects Drosophila associative olfactory short-term memory across 26 learning tasks. These tasks differ in the reinforcers and the amount of training, the life stage of the animals, in the predictive structure and associative timing of the task, in whether memory is expressed as an increase or decrease in odour preference, and in whether the learned behaviour is motivated by obtaining reward or avoiding/ escaping punishment. In adult flies, an improvement was observed for appetitive odour-sugar memories, whereas all tasks yielding aversive memory were unaffected. Strikingly, appetitive tasks that are not sugar-related, namely odour-shock extinction learning and punishment-relief associations, were either unaffected or even impaired, supporting the adaptive specificity hypothesis. In contrast, in 5-day-old larvae sugar-related appetitive associations were compromised, and the same was observed, to varying degrees, in larvae starved one day earlier and for aversive quinine associations, challenging the adaptive specificity hypothesis. Furthermore, we observed starvation-induced changes in locomotion and preference for a subset of the cues used in our study. Our results defy a simplistic interpretation in terms of the adaptive specificity hypothesis and call for case-by-case analyses of how starvation affects learning and behaviour.