Van De Poll Matthew N, van Swinderen Bruno
Queensland Brain Institute, The University of Queensland, St Lucia, QLD 4072, Australia.
J Exp Biol. 2025 Jun 1;228(11). doi: 10.1242/jeb.250165. Epub 2025 Jun 3.
During sleep, behavioral responsiveness to external stimuli is decreased. This classical definition of sleep has been applied effectively across the animal kingdom to identify this common behavioral state in a growing list of creatures, from mammals to invertebrates. Yet, it remains unclear whether decreased behavioral responsiveness during sleep is necessarily associated with decreased responsiveness in brain activity, especially in insects. Here, we performed long-term multichannel electrophysiology in tethered Drosophila melanogaster flies exposed continuously to repetitive visual stimuli. Flies were still able to sleep under these visual stimulation conditions, as determined by traditional immobility duration criteria for the field. Interestingly, we did not find any difference between responses to repetitive visual stimuli during sleep compared with wake when we recorded local field potentials (LFPs) across a transect of the fly brain from optic lobes to the central brain. However, we did find LFP responses to be altered when visual stimuli were variable and of lower probability, especially in the central brain. Central brain responses to less predictable or 'deviant' stimuli were lower during the deepest stage of sleep, a time of quiescence characterized by more regular proboscis extensions. This shows that the sleeping fly brain processes low-probability visual stimuli in a different way from more repeated stimuli, and presents Drosophila as a promising model for studying the potential role of sleep in regulating predictive processing.
在睡眠期间，对外部刺激的行为反应性会降低。睡眠的这一经典定义已在动物界广泛应用，以识别越来越多生物（从哺乳动物到无脊椎动物）中的这种常见行为状态。然而，睡眠期间行为反应性降低是否必然与大脑活动反应性降低相关，尤其是在昆虫中，仍不清楚。在此，我们对连续暴露于重复性视觉刺激下的系留黑腹果蝇进行了长期多通道电生理学研究。根据该领域传统的静止持续时间标准，果蝇在这些视觉刺激条件下仍能够睡眠。有趣的是，当我们记录从视叶到中枢脑的果蝇大脑横切面上的局部场电位（LFP）时，我们发现睡眠期间对重复性视觉刺激的反应与清醒时相比没有任何差异。然而，当视觉刺激多变且概率较低时，我们确实发现LFP反应发生了改变，尤其是在中枢脑。在睡眠最深阶段，即由更规律的喙伸展所表征的静止期，中枢脑对较不可预测或“异常”刺激的反应较低。这表明睡眠中的果蝇大脑以与更重复刺激不同的方式处理低概率视觉刺激，并将果蝇作为研究睡眠在调节预测性处理中潜在作用的一个有前景的模型。
