Olfactory oscillations: the what, how and what for

Abstract

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.

Figure 1

The range of oscillation types in the rat OB (top trace) and anterior piriform cortex (aPC; bottom trace); above each one the second LFP trace is a sonogram representation of the frequency structure from the OB segment. Coherence between the two traces is shown to the right of each sonogram, with the smallest dot representing the cutoff for significance (0.55) and values below that blank. (a) Rat attentive and breathing at a resting frequency (2 Hz). LFP shows a prominent theta oscillation coincident with inhalation cycle and gamma1 bursts initiating at the peak of inhalation. The theta frequency appears in dark red at the bottom. Because of the asymmetry of the respiratory wave, it shows a sweep between 5 and 1 Hz (over many inhalations, the 2 Hz frequency will survive the averaging). The two bursts are centered at 71 Hz (1st burst) and 78 Hz, with considerable spread in frequency within each burst. Coherence is high at gamma and respiratory frequencies. (b) Lower amplitude gamma1 bursts during grooming behavior; gamma2 episodes are evident between inhalations. Gamma2 bursts have a more consistent oscillation frequency (variable across individuals) than gamma1 bursts: 52 Hz here. Coherence is significant in the gamma2 frequency range. Very high frequency activity in the PC trace is from jaw movement electromyogram (EMG). (c) Extended gamma1 burst seen during odor sampling in criterion performance of a fine discrimination task (heptanone–octanone discrimination; the response to heptanone is shown). Coherence with PC is very low in the gamma1 range, indicating a decoupling of the normal oscillatory drive seen in part (a). (d) Beta oscillations recorded during odor sampling in a Go/No-Go task. The frequency of this oscillation begins low (probably owing to an underlying sensory evoked potential) and ends at ~20 Hz. Beta oscillation frequencies, like gamma2, are less variable within an animal than for gamma1. Coherence is very high in the beta band, with lower coherence in the respiratory frequency range. Data were digitized at 2016 Hz (Neuralynx Cheetah 32, Bozeman, MT, USA; NB Laboratories headstage; 1–475 Hz analog filter). Sonograms were made using a Gabor taper on a 2016 point window (padded with zeroes when necessary), stepped by 1 time point (Igor Pro 6.03-Wavemetrics, Lake Oswego, OR, USA). Power is dimensionless because data are normalized to zero mean and unit standard deviation and all four plots use the same power and coherence scales.

Figure 2

OB theta oscillations track the respiratory cycle during fast sniffing. The top trace is the theta band (low pass digital filter at 12 Hz) from the OB LFP; the bottom trace is EMG from the diaphragm; and the middle trace is a smoothed version of the EMG. One second of data sampled at 2016 Hz is shown.

Figure 3

Basic OB circuit, including points at which neuromodulators might affect oscillations (not all types and locations of receptors are shown here). Since we know most about the circuits involved in the gamma1 rhythm, the figure concentrates on the mitral–granule cell reciprocal synapse, which supports this oscillation. Receptors at the receptor neuron to mitral cell and juxtaglomerular cell synapses might affect the strength of the respiratory rhythm, input or sensory evoked potentials. Dopaminergic D₁ and D₂ receptors regulate the strength of inhibition at the reciprocal synapse and the strength of sensory input [67,68]. Noradrenergic receptors of several types at this synapse affect the excitability of both mitral and granule cells and the strength of inhibition, and they affect discrimination of closely related odorants [48,57]. Cholinergic action on granule cells decreases their firing rates but increases the release of GABA [69]. Glutamate receptors are of both AMPA and NMDA types (metabotropic receptors not shown). Abbreviations: dSA, deep short axon cell (GABAergic); GL, glomerulus; GR, granule cell (GABAergic); JG, juxtaglomerular cells (yellow is GABAergic and blue and yellow is both dopaminergic and GABAergic); MC, mitral cell (glutamatergic); ORN, olfactory receptor neuron axon (glutamatergic) [30].