Sniffing shapes the dynamics of olfactory bulb gamma oscillations in awake behaving rats

Abstract

Mammals actively sample the environment for relevant olfactory objects. This active sampling is revealed by rapid changes in respiratory rate that influence the olfactory input. Yet the role of sniffing in shaping the neural responses to odorants has not been elucidated. In the olfactory bulb (OB), odorant-evoked gamma oscillations reflect the synchronous activity of mitral/tufted cells, a proposed mechanism for odorant representation. Here we examined the effect of sniffing frequency on the odorant-evoked gamma oscillations in the OB. We simultaneously recorded the respiratory rate and the local field potential while rats performed a lick/no-lick olfactory discrimination task with low odorant concentrations. High-frequency sniffing (HFS) augmented the power of gamma oscillations, suggesting an increase in the sensitivity to odorants. By contrast, coupling of the gamma oscillations to the sniff cycle and the amplitude of individual bursts were not modified by the respiratory rate. However, HFS prolonged the overall response to odorants and increased the frequency of the gamma oscillations, indicating that HFS reduces the adaptation to continuous odorant stimulation. Therefore, the increase in gamma power during HFS is the result of more frequent gamma bursts and the extended response to odorants. As odorant discrimination can be performed in a single sniff, a reduction in the adaptation mediated by HFS of novel odorants may facilitate odorant memory formation for subsequent odorant identification. Finally, these results corroborate that olfactory sampling should be integrated to the study of odorant coding in behaving animals.