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, rewarding, 3) non-ethotypical, 4) repeated, yet
unstereotyped, and 5) free from stress1,2. Play-like behavior following these rules is
pervasive across the vertebrate subphylum2; recent studies in rats even identified and
characterized involved brain regions3,4. In invertebrates, sparse reports so far addressed
either social play in parasitoid wasps or spiders5,6, object play in bumblebees7, or are
anecdotal1. 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
pull8, hence such intentional passive motion could be sufficient to induce proprioceptive
stimulation externally9. 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.
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, rewarding, 3) non-ethotypical, 4) repeated, yet
unstereotyped, and 5) free from stress1,2. Play-like behavior following these rules is
pervasive across the vertebrate subphylum2; recent studies in rats even identified and
characterized involved brain regions3,4. In invertebrates, sparse reports so far addressed
either social play in parasitoid wasps or spiders5,6, object play in bumblebees7, or are
anecdotal1. 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
pull8, hence such intentional passive motion could be sufficient to induce proprioceptive
stimulation externally9. 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.
Original language | English |
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Journal | Current Biology |
Publication status | Accepted/In press - 14 Jan 2025 |
Keywords
- drosophila
- idiosyncratic behavior
- sensation seeking
- play
- locomotion
- efference copy
- corollary discharge
- exafference
- internal model
- body self