Abstract

Recent brain connectome studies have evidenced distinct and overlapping brain regions involved in processing olfactory perception. However, neural correlates of hypo- or anosmia in olfactory disorder patients are poorly known. Furthermore, the bottom-up and top-down processing of olfactory perception have not been well-documented, resulting in difficulty in locating the disease foci of olfactory disorder patients. The primary aim of this study is to characterize the bottom-up process of the neural dynamics across peripheral and central brain regions in anesthetized mice. We particularly focused on the neural oscillations of local field potential (LFP) in olfactory epithelium (OE), olfactory blub (OB), prefrontal cortex (PFC), and hippocampus (HC) during an olfactory oddball paradigm in urethane anesthetized mice. Odorant presentations evoked neural oscillations across slow and fast frequency bands including delta (1–4 Hz), theta (6–10 Hz), beta (15–30 Hz), low gamma (30–50 Hz), and high gamma (70–100 Hz) in both peripheral and central nervous systems, and the increases were more prominent in the infrequently presented odorant. During 5 s odorant exposures, the oscillatory responses in power were persistent in OE, OB, and PFC, whereas neural oscillations of HC increased only for short time at stimulus onset. These oscillatory responses in power were insignificant in both peripheral and central regions of the ZnSO4-treated anosmia model. These results suggest that olfactory stimulation induce LFP oscillations both in the peripheral and central nervous systems and suggest the possibility of linkage of LFP oscillations in the brain to the oscillations in the peripheral olfactory system.

Highlights

  • Olfactory dysfunction is a common condition, with a reported prevalence of 4 to 24.5% (Estrem and Renner, 1987; Murphy et al, 2002; Bramerson et al, 2004; Vennemann et al, 2008; Schubert et al, 2012)

  • The temporal profiles of powers show that the elevated powers persisted in olfactory epithelium (OE), olfactory blub (OB), and prefrontal cortex (PFC) during the stimulation period, while the change ceased early in HC (Supplementary Figure S2)

  • Concerning the emergence of peripheral nervous system neural oscillations along with central nervous system oscillations during odor stimulation, our results showed that OE oscillations from δ to high γ emerged during odor stimulation

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Summary

Introduction

Olfactory dysfunction is a common condition, with a reported prevalence of 4 to 24.5% (Estrem and Renner, 1987; Murphy et al, 2002; Bramerson et al, 2004; Vennemann et al, 2008; Schubert et al, 2012). Recent epidemiological studies have shown that self-reported olfactory dysfunction is more common in men than in women (Schubert et al, 2012), tends to increase with age (Doty et al, 1984a), and is related to smoking (Frye et al, 1990). The aetiologies of olfactory dysfunction are various (Doty, 2006), but are often classified as follows: (1) conductive impairment from the blockage of nasal airflow (e.g., rhinosinusitis and polyposis) (Deems et al, 1991), which happens in most patients with hyposmia or anosmia; and (2) sensorineural impairment from damage. The first type is peripheral olfactory dysfunction, which occurs following damage to the OE due to upper respiratory infections, among other causes (Deems et al, 1991; Suzuki et al, 2007). The dynamics of how the bottom-up signals of odorants propagate to the central brain regions are poorly known, limiting the diagnostic evaluation of hypo- or anosmia in olfactory disorder patients

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