Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system

Abstract

Oscillatory phenomena have been a focus of dynamical systems research since the time of the classical studies on the pendulum by Galileo. Fast cortical oscillations also have a long and storied history in neurophysiology, and olfactory oscillations have led the way with a depth of explanation not present in the literature of most other cortical systems. From the earliest studies of odor-evoked oscillations by Adrian, many reports have focused on mechanisms and functional associations of these oscillations, in particular for the so-called gamma oscillations. As a result, much information is now available regarding the biophysical mechanisms that underlie the oscillations in the mammalian olfactory system. Recent studies have expanded on these and addressed functionality directly in mammals and in the analogous insect system. Sub-bands within the rodent gamma oscillatory band associated with specific behavioral and cognitive states have also been identified. All this makes oscillatory neuronal networks a unique interdisciplinary platform from which to study neurocognitive and dynamical phenomena in intact, freely behaving animals. We present here a summary of what has been learned about the functional role and mechanisms of gamma oscillations in the olfactory system as a guide for similar studies in other cortical systems.

Fig. 1

Neuronal layers, types and circuitry of the OB. (a) Sagittal section through a rodent OB. The olfactory nerve has been removed, although in the anterior surface of the bulb some remnants can be seen. Glomerular (G) layer and mitral cell (MC) layer are seen clearly. Axons of mitral cells are stained in blue (Nissl stain). AOB: Accessory OB. D, V, R, C: Dorso-Ventral and Rostro-Caudal axes. (b) Main components of the OB neuronal network. Not all the described interactions are shown. Green and red arrows represent excitatory and inhibitory synaptic interactions, respectively. A mutual inhibition relationship has been proposed by some authors between granule cells. ORN: Olfactory receptor neuron; M/T: Mitral and Tufted cells; GR: granule cell; JG: juxtaglomerular cell; LOT: Lateral olfactory tract. (a) taken from (Elsaesser and Paysan 2007) (publisher: BioMed Central)

Fig. 2

Gamma and theta LFP oscillations recorded from the OB of an awake, freely behaving rat. The top (green) trace shows raw LFP recording (1–475 Hz). Middle trace shows recording filtered between 1–12 Hz, revealing the Theta oscillation. Bottom trace displays the recording filtered between 65–100 Hz, showing the gamma oscillation. The theta oscillation can be used as a proxy for the animal’s respiration cycle, where the rising phase of the oscillation corresponds to inspiration and the falling phase to expiration. Note the correlation between the theta phase and the onset of gamma bursts. Upward deflection corresponds to positive polarity

Fig. 3

Reciprocal dendrodendritic synapse between M/T and granule cells. Action potentials from ORNs arrive at glomeruli (gray circles) and excite (short green arrows) M/T cells. This depolarization propagates from the postsynaptic membrane through the entire cell (long green arrows), resulting in excitation of granule cells through glutamate liberation at the dendrodendritic synapse. The excitation of granule cells causes them to liberate GABA (red arrows), eliciting recurrent and lateral inhibition of M/T cells. Note that due to the geometry of the arrangement, the same dynamical interactions can be elicited by antidromic activation of M/T cells. GR: granule cell. OD, AD: antidromic and orthodromic directions. After Rall et al. (1966)

Fig. 4

Antidromically evoked LFPs in the rabbit OB at different depths (indicated in mm). Animal was anesthetized. GL: glomerular layer; EPL: External plexiform layer; MBL: Mitral layer; GRL: granule cell layer. From Rall and Shepherd (1968), used with permission

Fig. 5

Current source-density CSD analysis of LFP gamma oscillations in the OB of anesthetized rats. Current sources (blue tones) and sinks (red tones) are shown under different conditions. Recording depths are shown in each plot, and the corresponding cell layers are labeled in Ai. The top plots show results obtained by using three different kinds of M/T stimulation: antidromic, by stimulation of the lateral olfactory tract (Ai), orthodromic, by stimulation of the olfactory nerve (Aii), and centrifugal, by stimulation of pyriform cortex (Aiii). B shows the temporal evolution of the sources and sinks during a gamma oscillation. From Neville and Haberly (2003), used with permission

Fig. 6

Relationship between M/T spiking activity and LFP oscillation phase. (A) Mice OB slices, electrical stimulation of the olfactory nerve. The top traces show the simultaneous recording of extracellular action potentials from a M/T cell and LFPs, highlighting the relationship between the spiking time and the LFP phase. The star indicates the time of the stimulation. In the bottom plots, results are summarized for sixteen cells, showing the mean action potential number in a post stimulus time histogram (left) and M/T spike firing probability for different LFP phases. (B) Urethane-anesthetized rabbits, odorant stimulation. The top trace in (a) shows the duration of stimulation, the middle trace shows M/T spiking activity and bottom trace displays the LFP simultaneously measured. (b and c) show the relationship between M/T spiking activity and LFP phase, in (b) for one cell and in (c) for eleven cells. OLFP: Oscillatory LFP. (A) from Bathellier et al. (2006) and (B) from Kashiwadani et al. (1999), used with permission

Fig. 7

Picrotoxin abolition of odor-induced gamma LFP oscillations and olfactory discrimination impairment in honeybees. (A) Traces in (a) show the LFP signal during the presentation of the odor with (left) and without (right) previous application of picrotoxin (PCT). Power spectra correspondent to traces in (a) are shown in (b). (B) In (a) is shown the experimental training and testing protocol for the discrimination. (b) shows the conditioning protocol and the bees’ learning (in this paradigm, the odor is the unconditioned stimulus and it is paired with the proboscis extension, which corresponds to a conditioned response). (c) shows the behavioral differences between saline- and PCT-treated animals. C and S correspond to similar odors (aliphatic alcohols differing only in chain length) and D is the terpene geraniol. Note that PCT-treated bees cannot discriminate between C and S. Reprinted by permission from Macmillan Publishers Ltd.: Nature 390:70–74 (6 November 1997), copyright 1997

Fig. 8

Enhanced LFP gamma activity in the OB of ß3−/− mice. (A) Data shows four examples of raw tracings of OB LFP signals recorded from freely behaving animals during exploration of their cage. Gamma oscillations are seen in bursts of activity, much more prominent in the case of the mutant animals. From Nusser et al. (2001), used with permission. (B) Power spectra of OB LFP signals during exploratory behavior. Note the increase in power centered around 65 Hz for mutant animals. From Kay (2003), used with permission

Fig. 9

Intrinsic modulation of olfactory gamma LFP oscillation power in rats, matching the tasks demands. (A) LFP recordings during an olfactory discrimination task, showing OB (OB) and pyriform cortex (PC) raw signals (1–475 Hz) and gamma-filtered signal (65–100 Hz). (a) Corresponds to a ‘coarse’ discrimination task (dissimilar odorants) and (b) corresponds to a ‘fine’ discrimination (very similar odorants). (c) Shows the power spectra of the odor delivery period for the gamma band (indicated with colored bars in a and b) for both conditions. Note the enhanced power for the ‘fine’ condition. (B) Evolution of gamma power within sessions, for coarse and fine discriminations. From Beshel et al. (2007), used with permission

Fig. 10

Two different kinds of gamma oscillatory activity in the rat. (a) Power spectra from OB LFP recordings during an olfactory discrimination task. During the waiting period (prior to odor presentation) there is a low-frequency component of gamma activity, centered around 50 Hz, that is absent during odor sampling (‘sniffing’); from Kay (2003), used with permission. (b) LFP activity recorded from freely moving animals during three different behaviors. Green traces: raw data; middle traces: data filtered between 35–65 Hz (‘gamma 2’); bottom traces: data filtered between 65–100 Hz (‘gamma 1’). Note that during sniffing behavior the theta frequency is much higher (about 8 Hz) than during grooming or standing still (about 1 Hz). Note as well the absence of gamma 2 bursts during sniffing. Upward deflection corresponds to positive polarity