Odor modality is transmitted to cortical brain regions from the olfactory bulb

J Neurophysiol. 2023 Nov 1;130(5):1226-1242. doi: 10.1152/jn.00101.2023. Epub 2023 Oct 4.

Abstract

Odor perception is the impetus for important animal behaviors with two predominate modes of processing: odors pass through the front of the nose (orthonasal) while inhaling and sniffing, or through the rear (retronasal) during exhalation and while eating. Despite the importance of olfaction for an animal's well-being and that ortho and retro naturally occur, it is unknown how the modality (ortho vs. retro) is even transmitted to cortical brain regions, which could significantly affect how odors are processed and perceived. Using multielectrode array recordings in tracheotomized anesthetized rats, which decouples ortho-retro modality from breathing, we show that mitral cells in rat olfactory bulb can reliably and directly transmit orthonasal versus retronasal modality with ethyl butyrate, a common food odor. Drug manipulations affecting synaptic inhibition via GABAA lead to worse decoding of ortho versus retro, independent of whether overall inhibition increases or decreases, suggesting that the olfactory bulb circuit may naturally favor encoding this important aspect of odors. Detailed data analysis paired with a firing rate model that captures population trends in spiking statistics shows how this circuit can encode odor modality. We have not only demonstrated that ortho/retro information is encoded to downstream brain regions but also used modeling to demonstrate a plausible mechanism for this encoding; due to synaptic adaptation, it is the slower time course of the retronasal stimulation that causes retronasal responses to be stronger and less sensitive to inhibitory drug manipulations than orthonasal responses.NEW & NOTEWORTHY Whether ortho (sniffing odors) versus retro (exhalation and eating) is encoded from the olfactory bulb to other brain areas is not completely known. Using multielectrode array recordings in anesthetized rats, we show that the olfactory bulb transmits this information downstream via spikes. Altering inhibition degrades ortho/retro information on average. We use theory and computation to explain our results, which should have implications on cortical processing considering that only food odors occur retronasally.

Keywords: decoding accuracy; ethyl butyrate; firing rate model; retronasal olfaction; synaptic inhibition.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Nose / physiology
  • Odorants*
  • Olfactory Bulb / physiology
  • Olfactory Perception* / physiology
  • Rats
  • Smell / physiology

Associated data

  • figshare/10.6084/m9.figshare.14877780.v1