Abstract
Organisms quickly learn about their surroundings and display synaptic plasticity which is thought to be critical for their survival. For example, fruit flies Drosophila melanogaster exposed to highly enriched social environment are found to show increased synaptic connections and a corresponding increase in sleep. Here we asked if social environment comprising a pair of same-sex individuals could enhance sleep in the participating individuals. To study this, we maintained individuals of D. melanogaster in same-sex pairs for a period of 1 to 4 days, and after separation, monitored sleep of the previously socialized and solitary individuals under similar conditions. Males maintained in pairs for 3 or more days were found to sleep significantly more during daytime and showed a tendency to fall asleep sooner as compared to solitary controls (both measures together are henceforth referred to as “sleep-enhancement”). This sleep phenotype is not strain-specific as it is observed in males from three different “wild type” strains of D. melanogaster. Previous studies on social interaction mediated sleep-enhancement presumed ‘waking experience’ during the interaction to be the primary underlying cause; however, we found sleep-enhancement to occur without any significant increase in wakefulness. Furthermore, while sleep-enhancement due to group-wise social interaction requires Pigment Dispersing Factor (PDF) positive neurons; PDF positive and CRYPTOCHROME (CRY) positive circadian clock neurons and the core circadian clock genes are not required for sleep-enhancement to occur when males interact in pairs. Pair-wise social interaction mediated sleep-enhancement requires dopamine and olfactory signaling, while visual and gustatory signaling systems seem to be dispensable. These results suggest that socialization alone (without any change in wakefulness) is sufficient to cause sleep-enhancement in fruit fly D. melanogaster males, and that its neuronal control is context-specific.
Highlights
Sleep-like state is widely observed across animal kingdom, from simple nematodes to complex mammals; yet its advantages are not entirely clear [1]
These results suggest that 3 days of pair-wise interaction is enough to cause sleep-enhancement in males
Previous studies have suggested wake promoting l-LNv neurons to play a critical role in sleep-enhancement, whereas we found that both ablation as well as silencing of Pigment Dispersing Factor (PDF) neurons does not have any detectable impact on sleep-enhancement, which rules out the role of PDF neurons in sleep-enhancement resulting due to pair-wise social interaction between males
Summary
Sleep-like state is widely observed across animal kingdom, from simple nematodes to complex mammals; yet its advantages are not entirely clear [1]. In mammals as well as in Drosophila, sleep after a training session is essential for memory consolidation through synaptic potentiation [7,8,9]. In contextual fear conditioning in mice, sleep deprivation after a training session results in impaired memory consolidation [7]. In Drosophila, sleep helps in long term memory (LTM) formation through mass training, which under normal circumstances is not known to induce LTM [9]. Like many other organisms, sleep more during the early life stages, which is believed to help certain parts of their brain such as VAIv glomeruli to grow, and sleep deprivation during these stages results in impaired development of the VAIv glomeruli [11]
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