Behavioural and neurogenetic evidence for emotion primitives in the fruit fly Drosophila: insights from the Open Field Test

Abstract

Emotions, defined as transient states preparing organisms for adaptive responses, are thought to be based on evolutionarily conserved building blocks ("emotion primitives") that are present across mammalian and other vertebrate species. Whether and to which extent these building blocks are found in insects is largely undefined. In this study, we employ the open field test in fruit flies and focus on wall-following and total walking activity as behavioural indicators of emotion-like states. Wildtype and transgenic flies were subjected to various conditions, including social isolation, starvation, and exposure to anxiolytic substances prior to behavioural testing in the open field test. The results indicate that wall-following and total walking activity are modulated by these conditions, with generally increased wall-following observed under aversive stimuli and decreased values under positive conditions. Notably, the behaviour was consistent across different times of the day and independent of circadian rhythms. Genetic manipulation of neuromodulatory systems, such as serotonin, dopamine, and neuropeptide F, supports the role of these pathways in modulating emotion-like states in the fruit fly. Activation of reward-related neurons decreased wall-following, while inhibition increased it, aligning with known effects in mammalian models. Additionally, pharmacological treatments with ethanol and diazepam produced predictable changes in wall-following and total walking activity, reinforcing the validity of the open field test as a measure of emotion-like states in the fly. The findings suggest that Drosophila exhibits core emotion-like states, with wall-following and total walking activity serving as reliable indicators of emotional valence and arousal. Our results promote the use of Drosophila as a powerful genetic model to dissect the neuronal and neurochemical substrates of emotion primitives, shedding light on the evolution of basic emotional processing mechanisms.

Competing Interest Statement

The authors have declared no competing interest.