Reciprocal relationships between sleep and smell

Abstract

Despite major anatomical differences with other mammalian sensory systems, olfaction shares with those systems a modulation by sleep/wake states. Sleep modulates odor sensitivity and serves as an important regulator of both perceptual and associative odor memory. In addition, however, olfaction also has an important modulatory impact on sleep. Odors can affect the latency to sleep onset, as well as the quality and duration of sleep. Olfactory modulation of sleep may be mediated by direct synaptic interaction between the olfactory system and sleep control nuclei, and/or indirectly through odor modulation of arousal and respiration. This reciprocal interaction between sleep and olfaction presents novel opportunities for sleep related modulation of memory and perception, as well as development of non-pharmacological olfactory treatments of simple sleep disorders.

Keywords: fragrance; insomnia; memory; odor perception; olfaction; sleep.

FIGURE 1

Schematic of major circuits involved in sleep and waking. Major direct contributors to arousal and waking are the excitatory projections from the pedunculopontine tegmental nucleus (PPT) and the parabrachial nucleus (PB) to basal forebrain (BF) that projects broadly throughout the cortex, including the olfactory cortex. Neurons in the lateral hypothalamus (LH) contribute to inhibition of sleep promoting regions. Dopamine release by the periaqueductal grey (PAG) area directly contributes to waking, while histamine from the tuberomammillary nucleus (TMN), serotonin from the raphe nucleus (RN) and norepinephrine from the locus coeruleus (LC) have more modulatory roles in promoting cortical arousal. Sleep promoting regions include the preoptic area (POA), specifically the ventrolateral preoptic (VLPO) and median preoptic (MnPO) areas which send GABAergic projections to major components of the waking system.

FIGURE 2

Schematic of major olfactory system components (blue) and overlap with sleep related areas (purple). Odor information flows from the olfactory bulb (OB) to the piriform cortex (PCX). PCX direct projection targets include the mediodorsal nucleus of the thalamus (MDT), the orbitofrontal cortex (OFC), the amygdala (AMG), and regions of the lateral hypothalamus (LH). The olfactory system receives strong neuromodulatory input from the cholinergic basal forebrain (BF), serotonergic raphe nucleus (RN), and the noradrenergic locus coeruleus (LC). Importantly, neurons in the LH, BF, and LC have all been shown to also be odor responsive.

FIGURE 3

Summary schematic of some of the major bidirectional interactions between olfaction and sleep. Odors that can enhance arousal or stress will promote waking and/or delay sleep, duration, or quality. Conversely, odors that reduce arousal or stress will promote sleep. Sleep, in turn, can facilitate odor memory consolidation though it can reduce olfactory system sensitivity to ongoing odors. Finally, odors that reduce respiration rate can reduce activity in circuits promoting wakefulness leading to increased probability of sleep. During sleep, respiration rate and depth can impair odor access to sensory neurons contributing to reduce olfactory system responsiveness.