Long-term multichannel recordings in Drosophila flies reveal altered predictive processing during sleep compared with wake

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 perform 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 to
wake when we recorded local field potentials (LFP) 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 than more repeated
stimuli, and presents Drosophila as a promising model for studying the
potential role of sleep in regulating predictive processing.