Trends in Neurosciences
ReviewOlfactory oscillations: the what, how and what for
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.
References (69)
What do electrophysiological studies tell us about processing at the olfactory bulb level? J
Physiol. (Paris)
(2007)- et al.
Information processing in the olfactory systems of insects and vertebrates
Semin. Cell Dev. Biol.
(2006) - et al.
Slow-waves in the olfactory system: an olfactory perspective on cortical rhythms
Trends Neurosci.
(2006) - et al.
Pyriform cortex β-waves: odor-specific sensitization following repeated olfactory stimulation
Brain Res.
(2001) - et al.
Respiratory patterning of the rat olfactory bulb unit activity: nasal versus tracheal breathing
Neurosci. Lett.
(1990) Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs
Neuron
(2006)- et al.
Correlations between unit firing and EEG in the rat olfactory system
Brain Res.
(1990) Strong coupling between pyramidal cell activity and network oscillations in the olfactory cortex
Neuroscience
(2008)- et al.
Recent dynamics in olfactory population coding
Curr. Opin. Neurobiol.
(2001) - et al.
Temporal encoding of place sequences by hippocampal cell assemblies
Neuron
(2006)
Temporal structure in spatially organized neuronal ensembles – a role for interneuronal networks
Curr. Opin. Neurobiol.
Inhibition-based rhythms: experimental and mathematical observations on network dynamics
Int. J. Psychophysiol.
Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding
Neuron
Mechanisms of odor discrimination: neurophysiological and behavioral approaches
Trends Neurosci.
Speed-accuracy tradeoff in olfaction
Neuron
Response preparation and inhibition: the role of the cortical sensorimotor beta rhythm
Neuroscience
An argument for an olfactory thalamus
Trends Neurosci.
Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system
Cogn. Neurodyn.
Olfactory bulb gamma oscillations are enhanced with task demands
J. Neurosci.
Disruption of GABAA receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network
J. Neurophysiol.
Impaired odour discrimination on desynchronization of odour- encoding neural assemblies
Nature
An olfacto-hippocampal network is dynamically involved in odor-discrimination learning
J. Neurophysiol.
Sniffing controls an adaptive filter of sensory input to the olfactory bulb
Nat. Neurosci.
Theta oscillations and sensorimotor performance
Proc. Natl. Acad. Sci. U. S. A.
Sparse odor coding in awake behaving mice
J. Neurosci.
Olfactory computations and network oscillations
J. Neurosci.
Olfactory network dynamics and the coding of multidimensional signals
Nat. Rev. Neurosci.
Chemical factors determine olfactory system beta oscillations in waking rats
J. Neurophysiol.
Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input
J. Neurosci.
GABAergic inhibition at dendrodendritic synapses tunes γ oscillations in the olfactory bulb
Proc. Natl. Acad. Sci. U. S. A.
Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat
J. Neurophysiol.
γ-frequency excitatory input to granule cells facilitates dendrodendritic inhibition in the rat olfactory bulb
J. Neurophysiol.
Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb
J. Neurosci.
Circuit properties generating gamma oscillations in a network model of the olfactory bulb
J. Neurophysiol.
Cited by (245)
Drug-detecting bioelectronic nose based on odor cue memory combined with a brain computer interface
2024, Biosensors and BioelectronicsTraumatic brain injury-induced inflammatory changes in the olfactory bulb disrupt neuronal networks leading to olfactory dysfunction
2023, Brain, Behavior, and ImmunityCytoelectric coupling: Electric fields sculpt neural activity and “tune” the brain's infrastructure
2023, Progress in NeurobiologyObservation of respiration-entrained brain oscillations with scalp EEG
2023, Neuroscience Letters