Rapid Encoding and Perception of Novel Odors in the Rat

Abstract

To gain insight into which parameters of neural activity are important in shaping the perception of odors, we combined a behavioral measure of odor perception with optical imaging of odor representations at the level of receptor neuron input to the rat olfactory bulb. Instead of the typical test of an animal's ability to discriminate two familiar odorants by exhibiting an operant response, we used a spontaneously expressed response to a novel odorant—exploratory sniffing—as a measure of odor perception. This assay allowed us to measure the speed with which rats perform spontaneous odor discriminations. With this paradigm, rats discriminated and began responding to a novel odorant in as little as 140 ms. This time is comparable to that measured in earlier studies using operant behavioral readouts after extensive training. In a subset of these trials, we simultaneously imaged receptor neuron input to the dorsal olfactory bulb with near-millisecond temporal resolution as the animal sampled and then responded to the novel odorant. The imaging data revealed that the bulk of the discrimination time can be attributed to the peripheral events underlying odorant detection: receptor input arrives at the olfactory bulb 100–150 ms after inhalation begins, leaving only 50–100 ms for central processing and response initiation. In most trials, odor discrimination had occurred even before the initial barrage of receptor neuron firing had ceased and before spatial maps of activity across glomeruli had fully developed. These results suggest a coding strategy in which the earliest-activated glomeruli play a major role in the initial perception of odor quality, and place constraints on coding and processing schemes based on simple changes in spike rate. Author Summary. Olfactory stimuli elicit temporally complex patterns of activity across groups of receptor neurons as well as across central neurons. It remains unclear which parameters among these complex activity patterns are important in shaping odor perception. To address this issue, we imaged from the olfactory bulb of awake rats as they detected and responded to odorants. We used a spontaneously expressed response to novel odorants—exploratory sniffing—as a behavioral measure of odor perception. This assay allowed us to measure the speed with which rats perform simple odor discriminations by monitoring changes in respiration. Rats discriminated a novel odorant from a learned one in as little as 140 ms. Simultaneously imaging the sensory input to the olfactory bulb carried by receptor neurons revealed that the bulk of the response time is due to the peripheral events underlying odorant detection (inhalation and receptor neuron activation), leaving only 50–100 ms for central processing and response initiation. In most trials, responses to a novel odorant began before the initial barrage of input had ceased and before spatial patterns of input to the bulb had fully developed. These results suggest a coding strategy in which the earliest inputs play a major role in the initial perception of odor quality and place constraints on coding schemes based on simple changes in firing rate. Imaging the olfactory bulb of awake rats reveals that odor discrimination occurs about 100 ms after sensory input reaches the brain, sharply limiting the role that spike rate and temporal integration can play in coding odor identity.