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, 115 (5), 2294-302

Odors Enhance Slow-Wave Activity in Non-Rapid Eye Movement Sleep

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Odors Enhance Slow-Wave Activity in Non-Rapid Eye Movement Sleep

Ofer Perl et al. J Neurophysiol.

Abstract

Most forms of suprathreshold sensory stimulation perturb sleep. In contrast, presentation of pure olfactory or mild trigeminal odorants does not lead to behavioral or physiological arousal. In fact, some odors promote objective and subjective measures of sleep quality in humans and rodents. The brain mechanisms underlying these sleep-protective properties of olfaction remain unclear. Slow oscillations in the electroencephalogram (EEG) are a marker of deep sleep, and K complexes (KCs) are an EEG marker of cortical response to sensory interference. We therefore hypothesized that odorants presented during sleep will increase power in slow EEG oscillations. Moreover, given that odorants do not drive sleep interruption, we hypothesized that unlike other sensory stimuli odorants would not drive KCs. To test these hypotheses we used polysomnography to measure sleep in 34 healthy subjects (19 women, 15 men; mean age 26.5 ± 2.5 yr) who were repeatedly presented with odor stimuli via a computer-controlled air-dilution olfactometer over the course of a single night. Each participant was exposed to one of four odorants, lavender oil (n = 13), vetiver oil (n = 5), vanillin (n = 12), or ammonium sulfide (n = 4), for durations of 5, 10, and 20 s every 9-15 min. Consistent with our hypotheses, we found that odor presentation during sleep enhanced the power of delta (0.5-4 Hz) and slow spindle (9-12 Hz) frequencies during non-rapid eye movement sleep. The increase was proportionate to odor duration. In addition, odor presentation did not modulate the occurrence of KCs. These findings imply a sleep-promoting olfactory mechanism that may deepen sleep through driving increased slow-frequency oscillations.

Keywords: odor; olfaction; sleep; smell.

Figures

Fig. 1.
Fig. 1.
Sleep and stimulation patterns. A: number of trials (primary axis) and total sleep time (black markers, secondary axis). Bar color denotes the type of odor used per subject. B: distribution of sleep stages for all subjects who participated in the study.
Fig. 2.
Fig. 2.
Odor-induced brain modulation in sleep: power percent change in a 30-s time window following odor administration during nocturnal human sleep (black line) and “no odor” condition (gray line) during non-rapid eye movement (NREM, N2+N3; A) and rapid eye movement (REM; B) sleep. Error bars are SE. **P < 0.005.
Fig. 3.
Fig. 3.
Odor-induced brain modulation in sleep was independent of mild trigeminality: power percent change in a 30-s time window after trigeminal odor administration (black line) and olfactory odor administration (gray line) during NREM sleep. Error bars are SE. *P < 0.05.
Fig. 4.
Fig. 4.
Odor-induced brain modulation in sleep was dependent on odor duration. A–C: power percent change spectrograms of 30-s time window after odor administration for 20 s (A), 10 s (B), and 5 s (C) during NREM sleep. Red line indicates offset of the odor administration. D–F: power percent change in the delta (0.5–4 Hz) frequency band in 6 time windows of 5, 10, 15, 30, 45, and 60 s after odor administration for 20 s (D), 10 s (E), and 5 s (F) during NREM sleep. G–I: power percent change in the slow spindle (9–12 Hz) frequency band in 6 time windows of 5, 10, 15, 30, 45, and 60 s after odor administration for 20 s (G), 10 s (H), and 5 s (I) during NREM sleep. Error bars are SE. *P < 0.05.
Fig. 5.
Fig. 5.
Odor administration in sleep did not modulate K complex (KC) occurrence: scatterplots of the occurrence of KCs in 30-s time window before odor onset (y-axis) and after odor onset (x-axis) in all trials (A), 5-s odor administration trials (B), 10-s odor administration trials (C), and 20-s odor administration for trials (D). Diagonal line is a unit slope line, and each data point represents a subject. If a dot is located above the line it means that the average number of KCs before odor onset was larger than after odor onset in that subject.

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