State-dependent olfactory processing in freely behaving mice

• Published in: Cell reports (Cambridge) 2022-03, Vol.38 (9), p.110450-110450, Article 110450
• Main Authors: Schreck, Mary R., Zhuang, Liujing, Janke, Emma, Moberly, Andrew H., Bhattarai, Janardhan P., Gottfried, Jay A., Wesson, Daniel W., Ma, Minghong
• Format: Article
• Language: English
• Subjects: Animals; local field potential; mediodorsal thalamus; Mice; olfactory bulb; Olfactory Bulb - physiology; Olfactory Cortex; Olfactory Pathways - physiology; optogenetics; orbitofrontal cortex; piriform cortex; sensory gating; single-unit recording; sleep; Smell - physiology; Wakefulness - physiology
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.110450

Decreased responsiveness to sensory stimuli during sleep is presumably mediated via thalamic gating. Without an obligatory thalamic relay in the olfactory system, the anterior piriform cortex (APC) is suggested to be a gate in anesthetized states. However, olfactory processing in natural sleep states remains undetermined. Here, we simultaneously record local field potentials (LFPs) in hierarchical olfactory regions (olfactory bulb [OB], APC, and orbitofrontal cortex) while optogenetically activating olfactory sensory neurons, ensuring consistent peripheral inputs across states in behaving mice. Surprisingly, evoked LFPs in sleep states (both non-rapid eye movement [NREM] and rapid eye movement [REM]) are larger and contain greater gamma-band power and cross-region coherence (compared to wakefulness) throughout the olfactory pathway, suggesting the lack of a central gate. Single-unit recordings from the OB and APC reveal a higher percentage of responsive neurons during sleep with a higher incidence of suppressed firing. Additionally, nasal breathing is slower and shallower during sleep, suggesting a partial peripheral gating mechanism. [Display omitted] •OSN stimulations evoke larger olfactory LFPs in NREM and REM sleep than in wakefulness•Larger responses in sleep suggest the lack of a central gate in the olfactory pathway•More OB and APC units respond in NREM with a higher incidence of suppressed firing•Slower and shallower breathing could partially gate olfactory input in sleep Schreck et al. examine how the olfactory system responds to the same peripheral stimulus during natural sleep and wake in mice. Larger responses along the pathway during sleep suggest the lack of a central gate, but slower and shallower breathing may act as a partial peripheral gate to reduce olfactory input.