Olfactory system oscillations across phyla

Abstract

Neural oscillations are ubiquitous in olfactory systems of mammals, insects and molluscs. Neurophysiological and computational investigations point to common mechanisms for gamma or odor associated oscillations across phyla (40-100Hz in mammals, 20-30Hz in insects, 0.5-1.5Hz in molluscs), engaging the reciprocal dendrodendritic synapse between excitatory principle neurons and inhibitory interneurons in the olfactory bulb (OB), antennal lobe (AL), or procerebrum (PrC). Recent studies suggest important mechanisms that may modulate gamma oscillations, including neuromodulators and centrifugal input to the OB and AL. Beta (20Hz) and theta (2-12Hz) oscillations coordinate activity within and across brain regions. Olfactory beta oscillations are associated with odor learning and depend on centrifugal OB input, while theta oscillations are strongly associated with respiration.

Figure 1. Rhythms in the mammalian olfactory bulb

A. 1/f power spectrum with deviations for theta beta and gamma rhythms from rat OB. B. Gamma and theta rhythms recorded from the rat OB. Seven respiratory cycles are shown by the low frequency high amplitude wave in which the peak is the end of inhalation. The gamma rhythm begins at the peak with a high frequency oscillation giving way to a lower frequency one, sweeping form above 90 Hz to near 70 Hz. Top panel is the LFP trace and bottom panel is a wavelet spectrogram of the gamma band. C. LFP theta rhythms are coherent with respiratory drive at all waking respiratory frequencies. Left: OB LFP with theta filtered signal overlaid. The diaphragm EMG signal is rectified and smoothed, which shows the similarity with the simultaneously recorded OB theta rhythm. Right: Coherence between the two signals from one rat (histogram of respiratory frequencies on bottom of plot); horizontal line is the significance floor for coherence. Figure modified from [47] with permission. D. Gamma2 example from the rat OB. During slower respiration in alert rats, a low frequency high amplitude bursts in the 50–60 Hz range are seen. Wavelet spectrogram is shown and the frequency of bursts is lower than the end of the gamma sweep in A. E. Beta rhythm example recorded from the mouse OB in response to sniffing a highly volatile odor as in [55]. Wavelet spectrograms in the gamma and beta bands below (color scale in top is 1/10 that of the bottom to emphasize bursts).

Figure 2. Olfactory systems from 3 phyla

A. The mammalian central olfactory system begins with the OB, which receives olfactory nerve input from the olfactory epithelium (OE) in the glomeruli around the periphery of the bulb. Primary olfactory cortex is primarily represented by the anterior olfactory nucleus (AON) [64]. The pyriform cortex (PC) is a higher order sensory association cortex [65,66], but it is often referred to as primary olfactory cortex. The OB also projects to the multimodal entorhinal cortex (EC), which sends fibers into the hippocampus (HPC), and the amygdala (amyg) among other limbic and subcortical areas. The PC projects to the EC, hypothalamus and thalamus, as well as other higher order areas. Most OB connections to other brain regions are bidirectional. Centrifugal projections to the OB synapse primarily onto GABAergic GCs in the deep layers, except for the AON, which targets superficial juxtaglomerular cells and mitral cells [67]. (Figure adapted from [68].) B. The honeybee central olfactory system begins with antennal nerve (AN) input to the antennal lobe (AL) projection neurons in peripheral glomeruli. AL neurons project to the mushroom body (MB), a higher order multimodal area, and the lateral horn (LH). Descending modulatory input associated with appetitive state comes from the VUM-mx optopaminergic neuron in the subesophogeal ganglion (SOG). (Figure adapted from [69]). C. The limax cerebral ganglion receives olfactory nerve (ON) input to glomeruli in the procerebrum (PC). The PC also receives input from the medial lip nerve (MLN) in the inferior nose. (Figure adapted from [15] with permission.) D. Odor evoked oscillations (~20 Hz) are recorded in the locust mushroom body (MB) but are produced by axon terminals from the antennal lobe (AL) projection neurons (PN). Simultaneously recorded PN shows depolarization, odor evoked spikes and subthreshold oscillations. (Figure adapted from [26], with permission). E. Procerebral lobe oscillations in limax showing the <1Hz oscillation typical of this species. (Figure adapted from [15] with permission.)

Figure 3. A. Olfactory bulb circuitry associated with oscillations

Over the past few years, the canonical picture of OB circuitry has changed and some of the changes may have implications on mechanism and modification of OB oscillations: 1) Olfactory nerve input (not shown) targets external tufted (ET) cells directly (and possibly all tufted cells within glomeruli [31]) and then MT cells via excitatory inputs from ETs and inhibitory relays from ETs to periglomerular (PG) cells (not shown) to MT cells. ETs fire in bursts that can match the respiratory rhythm and may support theta oscillations [70]. One population of GABAergic deep short axon cells (dSAC) target PG cells [36]. Pyriform cortex input targets dSACs [37]. B. Reciprocal synapse as shown in the red dashed circle in A is on the distal dendrites of GCs and may support local graded inhibition through AMPA receptors with ~4.2 ms rise times [17]. This mechanism may support gamma oscillations independent of GC spikes [21]. NMDA and AMPA receptors are present on GCs at most synapses. About 25% are NMDA silent and a very small number are AMPA silent. GABAA receptors mediate inhibition of MTs. Synapses proximal to the GC soma from centrifugal axon fibers also have NMDA and AMPA receptors at most of these synapses (dashed black ovals). Activation of GCs by stimulating these fibers produces GABA release at the reciprocal synapse with faster rise times (1.3 ms). Additional abbreviations: GL- glomerular layer, EPL- external plexiform layer, MCL- mitral cell layer, GCL-granule cell layer.