Review
Olfactory oscillations: the what, how and what for

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Olfactory system oscillations play out with beautiful temporal and behavioral regularity on the oscilloscope and seem to scream ‘meaning’. Always there is the fear that, although attractive, these symbols of dynamic regularity might be just seductive epiphenomena. There are now many studies that have isolated some of the neural mechanisms involved in these oscillations, and recent work argues that they are functional and even necessary at the physiological and cognitive levels. However, much remains to be done for a full understanding of their functions.

Introduction

The various types of oscillations seen in the olfactory bulb (OB; see Glossary) local field potential (LFP) differ in frequency and in the circuits and behavioral circumstances that produce them. The best studied are gamma oscillations, which occupy the higher end of the olfactory LFP frequency range (∼70 Hz in rats and mice), are evoked by sensory stimulation and are initiated at the end of the inhalation cycle, riding the crest of the respiratory (theta) wave [1]. The power of odor-evoked gamma oscillations is associated with successful discrimination of closely related odorants 2, 3, 4. Both odor-evoked gamma and beta (∼20 Hz in rats) oscillations have been associated with odor learning 2, 5, and there is some evidence that the oscillation type and circuit could depend on the cognitive task 2, 6. There are many questions remaining to be answered about olfactory theta (∼1–12 Hz), beta (∼15–30 Hz) and gamma (∼40–100 Hz) frequency bands.

Oscillations in these frequency bands have been associated with sensory processing in other systems and with network properties in the hippocampus. However, frequencies can be deceiving, with even odor-evoked gamma oscillation frequencies varying widely across species [1]. Translating what has been learned about olfactory oscillations to other cortical systems, we argue that oscillations must be defined by multiple factors to make similarity arguments across systems and species.

Section snippets

What are the different rhythms?

A power spectrum of the rat OB LFP shows three distinct frequency bands corresponding to three classes of behavioral phenomena (Figure 1). Theta oscillations, so named because they overlap in frequency with hippocampal theta oscillations, are driven by sensory input and are also called respiratory oscillations [7]. Gamma oscillations are the fastest oscillations described in the olfactory system and are evoked by sensory input within a single inhalation–exhalation cycle. Beta oscillation

How do the rhythms come about?

Frequencies are only useful for assigning an identity to oscillatory phenomena within a species and often within a single individual because numbers vary across species and between individuals. Therefore, it is important to know the underlying mechanisms, sources and associated behavioral markers of oscillations, in addition to their relative frequency bands. This enables us to transition from a simple number-based taxonomy to a functional representation of oscillatory events.

What might the oscillations be good for?

Functional studies of cortical oscillations are more difficult than those that address their mechanisms, often requiring ablation of the oscillatory mechanism in awake-behaving animals. Many of these ablations interrupt more than the oscillation so the data must be interpreted with caution. However, in a few circumstances a strong functional argument can be made (see gamma oscillation section later). The remaining functional arguments for olfactory oscillations are still in the early stages and

Conclusions

It has been nearly seventy years since the first publication describing odor-evoked OB oscillations, and in that time we have made substantial progress in understanding the various oscillatory modes and their mechanistic and functional roles. We do not yet know whether all increases in gamma1 relate to increased discrimination ability, nor do we know the mechanisms for changing the strength of gamma1 oscillations online; neuromodulators and centrifugal synaptic input from other olfactory areas

Acknowledgements

We thank Donald Frederick for supplying some of the data for Figure 1 and Matt Wachowiak for helpful comments on the manuscript. L.M.K., D.R-L., C.M., J. Brea and N.K. were supported by the National Institute on Deafness and Other Communication Disorders (NIDCD; www.nidcd.nih.gov) R01 DC007995 (CRCNS grant). C.M. was also supported by a Fyssen Foundation fellowship (www.fondation-fyssen.org). J. Beshel was supported by a NIDCD pre-doctoral fellowship F31DC008467.

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