Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks?

Abstract

Olfactory processing in behaving animals, even at early stages, is inextricable from top down influences associated with odor perception. The anatomy of the olfactory network (olfactory bulb, piriform, and entorhinal cortices) and its unique direct access to the limbic system makes it particularly attractive to study how sensory processing could be modulated by learning and memory. Moreover, olfactory structures have been early reported to exhibit oscillatory population activities easy to capture through local field potential recordings. An attractive hypothesis is that neuronal oscillations would serve to "bind" distant structures to reach a unified and coherent perception. In relation to this hypothesis, we will assess the functional relevance of different types of oscillatory activity observed in the olfactory system of behaving animals. This review will focus primarily on two types of oscillatory activities: beta (15-40 Hz) and gamma (60-100 Hz). While gamma oscillations are dominant in the olfactory system in the absence of odorant, both beta and gamma rhythms have been reported to be modulated depending on the nature of the olfactory task. Studies from the authors of the present review and other groups brought evidence for a link between these oscillations and behavioral changes induced by olfactory learning. However, differences in studies led to divergent interpretations concerning the respective role of these oscillations in olfactory processing. Based on a critical reexamination of those data, we propose hypotheses on the functional involvement of beta and gamma oscillations for odor perception and memory.

Keywords: behavior; beta and gamma oscillations; odor learning; olfactory bulb; piriform cortex.

Figure 1

Odor stimulation modifies beta (15–35 Hz) and gamma (60–90 Hz) oscillations in the olfactory bulb. Example of LFP traces recorded in the olfactory bulb in freely moving mice. (A) Raw LFP signal (0.1–300 Hz) on first row is filtered in the theta (1–10 Hz) and the gamma (60–90 Hz) bands, showing the close relation between gamma bursts and the respiratory modulation. (B) Raw LFP signal (0.1–300 Hz) and corresponding time-frequency power representation in a mouse conditioned in a Go/No-Go task. Time-frequency plot was obtained based on Morlet wavelet analysis. It represents the power of the signal (as indicated by the color scale) as a function of time (x-axis) for each frequency (y-axis). Odorant onset is indicated by the vertical red arrow. Note that odor elicits an overall decrease in the gamma band and an increase in the beta band power.

Figure 2

Odor discrimination in two different behavioral tests led to distinct rhythms in the olfactory bulb. Example of raw LFP traces recorded in the olfactory bulb during a criterion session of discrimination between two alcohols (hexanol and heptanol) in two different paradigms: (A) a two-alternative choice test (Beshel et al., 2007) or (B) a Go/No-Go test (Martin et al., 2007). The two tests are schematized on the top. The main difference is that both odors are rewarded in the 2 alternative-choice whereas one odor is not rewarded in the Go/No-Go. In both cases, the same odor concentration is delivered. Odorants are generated in glass test tubes by bubbling air (100 ml/min) through a column of pure odorant and injecting the odorized air into a carrier air stream (400 ml/min) via a computer-controlled olfactometer achieving ~20% saturated vapor. LFPs recorded during odorant sampling periods are displayed, red arrows pointed out odorant onset. As underlined by shaded regions, in the two-alternative choice test, odors evoke high gamma power (65–85 Hz) whereas in the Go/No-Go context, odorant sampling is associated with a strong beta wave (15–40 Hz). It has to be noted that both rewarded and unrewarded odors trigger beta rhythm in the Go/No-Go test.

Figure 3

Schematic illustration of hypotheses for the generation of beta (15–35 Hz) and gamma (60–90 Hz) rhythms in the olfactory bulb and the piriform cortex in awake behaving animals. Example of raw LFP traces recorded (A) in the MOB in the absence of olfactory stimulation and (B) in MOB and two different regions of the PCx before learning and (C) after learning during a conditioned discrimination paradigm (Go/No-Go). a–c: Corresponding schematic representation of MOB and PCx interconnected networks and centrifugal modulation. The level of neuromodulation is represented by the red arrow on the left, the level of cortical feedback by green arrow on the right. (A) Spontaneous activity: in the absence of olfactory stimulation. Observe the regular theta respiratory modulation (around 2 Hz) and the associated bursts of gamma activity (60–90 Hz). See also in (B) and (C) the portion just preceding the odorant sampling (green square area) how the gamma bursts decrease in the posterior part of the PCx compare to the MOB and anterior part of PCx. a: In the absence of olfactory stimulation, the level of activation in both networks is weak and variable and both structures are dominated by theta and gamma activity. Gamma activity is transmitted from the MOB to the PCx. (B) Before learning: during odorant sampling, occurrence of gamma bursts is reduced but recovered after the animal has left the odor port. b: During this phase, a population of mitral cells of the MOB becomes active, this input is transmitted to a corresponding population of pyramidal cells. Both neuromodulatory and cortical feedback are exerted on the networks. However, no real coordination is set up in the network. (C) During training: In addition to a strong and sustained decrease in gamma activity, a clear beta oscillation is observed in the MOB and two regions of PCx associated to odorant sampling. c: During this phase, we propose that both assemblies of active mitral cells and pyramidal cells reinforce their connections. The result could be a more efficient and rapid transfer of olfactory information. This coordination is under the influence of both cortical feedback and neuromodulatory fibers as suggested by the results we observed with lidocaine inactivation of the peduncle (Martin et al., 2006). Once synaptic contacts are established, if the training is maintained to get over training, the amplitude of beta oscillatory activity decreases. On the contrary, if the animal is left in his home cage for a long interval without training and tested again, both structures exhibit a very strong beta oscillatory activity.