Precise olfactory responses tile the sniff cycle

Abstract

In terrestrial vertebrates, sniffing controls odorant access to receptors, and therefore sets the timescale of olfactory stimuli. We found that odorants evoked precisely sniff-locked activity in mitral/tufted cells in the olfactory bulb of awake mouse. The trial-to-trial response jitter averaged 12 ms, a precision comparable to other sensory systems. Individual cells expressed odor-specific temporal patterns of activity and, across the population, onset times tiled the duration of the sniff cycle. Responses were more tightly time-locked to the sniff phase than to the time after inhalation onset. The spikes of single neurons carried sufficient information to discriminate odors. In addition, precise locking to sniff phase may facilitate ensemble coding by making synchrony relationships across neurons robust to variation in sniff rate. The temporal specificity of mitral/tufted cell output provides a potentially rich source of information for downstream olfactory areas.

Intermediate intrinsic diversity enhances neural population coding

“…S3C). We note that the large range and diversity of firing rates observed among the MCs here is concordant with those found in vivo (26).…”

“…Alternatively, stimuli might be best encoded by groups of heterogeneous neurons, suggesting that maximizing the representation of temporal features of the stimuli is important (12,27). We specifically chose to study how diverse groups collectively represent an identical stimulus to mimic features of the olfactory bulb, where 25-50 sister MCs projecting to the same glomerulus (5) each receive highly correlated stimulus-and respiration-driven synaptic input (26,(28)(29)(30).…”

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

“…Following realignment, many cells showed clear odor responses with precise firing within the sniff cycle (16,17). Fig.…”

“…16; 60% at 2% dilution in ref. 17). Given that some cells do not respond during the first breath, but respond afterward, we calculated how many cell-odor pairs responded during the first breath alone (16%, 85/516), second breath alone (15%, 79/516), or both (20%, 108/516; Fig.…”

“…Others have measured the output of ORNs, by imaging glomeruli, and found that the response is gated by each breath and that the amplitude decreases with time (13,15). The importance of breath segmentation for M/T cells has recently been shown in awake subjects, where neurons respond with precise, phasic firing patterns (16)(17)(18). However, these recordings have focused on how information is represented during the first breath, as rodents can identify odors in a single breath (19)(20)(21).…”