The Role of Spike Timing in Odor Coding During Sniffing

Perception is shaped by active processes of stimulus acquisition. During exploration, many animals exhibit rhythmic and stereotyped sniffing in the theta frequency range (5-12 Hz), distinct from the slow, passive breathing that occurs during restful states (1-2 Hz). The olfactory bulb is the exclusive recipient of output from the nose. Mitral and tufted cells are the principal neurons of the olfactory bulb, forming the only output pathway. It is not known how mitral and tufted cells represent odors during natural sampling behavior. I used a combination of extracellular single-unit recording and psychophysics in behaving rats to address this issue. Through the use of two behavioral paradigms, odor responses were analyzed across distinct regimes of sampling behavior. During rapid sniffing, an analysis of the information that could be extracted from the response of a population of neurons revealed that the spike trains were most informative in their fine-scale fluctuations that occurred on a 20-40 ms timescales. To examine the behavioral relevance of these patterns, I examined whether the patterning of responses were related to the animals' decision making. This was indeed the case, as fine-scale response activity was correlated with the animals' reaction times on a trial-by-trial basis: the responses were more informative on trials in which only a single sniff was used. How robust is this code was to gross changes in sampling behavior? A code based on the fine-scale pattern of activity over the first 100 ms of inhalation was the most conserved between slow breathing and rapid sniffing. Finally, I evaluated the structure of odor responses across multiple sniffs during odor discrimination. The second sniff of an odor produced reliable responses locked to inhalation that were maximally informative over fine timescales, and could be discriminated nearly as accurately as responses from single-sniff trials. These results provide strong evidence in support of the notion that inhalation-coupled spike timing represents the neural code of mitral and tufted cells that is utilized by downstream structures to evaluate odor identity and guide behavioral response.