Play-like behavior exhibited by the vinegar fly Drosophila melanogaster.

Abstract

Anecdotal accounts about animals repeatedly exposing themselves to sources of passive movement by engaging with swings, slides, or carousels are generally assumed to be "play." Criteria for play-like behavior require the activity to be (1) of no immediate relevance for survival; (2) voluntary, intentional, and rewarding; (3) non-ethotypical; (4) repeated, yet unstereotyped; and (5) free from stress.^1,2 Play-like behavior following these rules is pervasive across the vertebrate subphylum²; recent studies in rats even identified and characterized the involved brain regions.^3,4 In invertebrates, sparse reports have so far addressed either social play in parasitoid wasps or spiders,^5,6 object play in bumblebees,⁷ or are anecdotal.¹ Contrary to social play or object play, which are thought to train social interaction or muscle/motor skills, respectively, a convincing hypothesis of the adaptive value of voluntary passive movement play-like behavior is currently lacking in any organism. Like other animals, flies are highly sensitive to the direction of gravitational pull,⁸ hence such intentional passive motion could be sufficient to induce proprioceptive stimulation externally.⁹ Here, we identify voluntary spinning on a carousel as idiosyncratic play-like behavior in the vinegar fly Drosophila melanogaster: while some flies show spontaneous avoidance, others actively seek stimulation, engaging in repeated, prolonged visits to the carousel. We propose that animals voluntarily expose themselves to external forces, thus intentionally receiving exafferent stimulation. This deliberate, yet indirect, proprioceptive stimulation provides an efficient way to improve self-perception via internal model training and shaping multisensory integration. Importantly, this theoretical framework can now be tested empirically in flies. VIDEO ABSTRACT.