Abstract

Respiration plays an essential role in odor processing. Even in the absence of odors, oscillating excitatory and inhibitory activity in the olfactory bulb synchronizes with respiration, commonly resulting in a burst of action potentials in mammalian mitral/tufted cells (MTCs) during the transition from inhalation to exhalation. This excitation is followed by inhibition that quiets MTC activity in both the glomerular and granule cell layers. Odor processing is hypothesized to be modulated by and may even rely on respiration-mediated activity, yet exactly how respiration influences sensory processing by MTCs is still not well understood. By using optogenetics to stimulate discrete sensory inputs in vivo, it was possible to temporally vary the stimulus to occur at unique phases of each respiration. Single unit recordings obtained from the mitral cell layer were used to map spatiotemporal patterns of glomerular evoked responses that were unique to stimulations occurring during periods of inhalation or exhalation. Sensory evoked activity in MTCs was gated to periods outside phasic respiratory mediated firing, causing net shifts in MTC activity across the cycle. In contrast, odor evoked inhibitory responses appear to be permitted throughout the respiratory cycle. Computational models were used to further explore mechanisms of inhibition that can be activated by respiratory activity and influence MTC responses. In silico results indicate that both periglomerular and granule cell inhibition can be activated by respiration to internally gate sensory responses in the olfactory bulb. Both the respiration rate and strength of lateral connectivity influenced inhibitory mechanisms that gate sensory evoked responses.

Highlights

  • Olfaction relies on respiration to bring odor molecules to the nasal epithelium to initiate sensory transduction in olfactory sensory neurons

  • Our in vivo work demonstrates some of the first spatiotemporal maps of mitral/tufted cells (MTCs) receptive fields [18, 41,42,43] and importantly the corresponding temporal changes that occur across specific phases of respiration

  • We provide an effective method of subtracting respiration-coupled activity to isolate glomerular regions associated with evoking excitation and inhibition of MTCs

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Summary

Introduction

Olfaction relies on respiration to bring odor molecules to the nasal epithelium to initiate sensory transduction in olfactory sensory neurons. In this way the respiratory cycle controls temporal periods of odor stimulation, which enforce rhythmic activity throughout the bulbar neural circuit [1, 2]. Rhythmic patterns of activity can be initiated in the absence of odor stimulation during inhalation when mechanoreceptors in olfactory sensory neurons are PLOS ONE | DOI:10.1371/journal.pone.0168356. Laboratory, funded by NIH grants: RR19895 and RR029676-01. We are grateful for the Neuroscience Gateway (NSG) Portal supported by the National Science Foundation

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