Testing the sorption hypothesis in olfaction: a limited role for sniff strength in shaping primary odor representations during behavior.

The acquisition of sensory information during behavior shapes the neural representation, central processing, and perception of external stimuli. In mammals, a sniff represents the basic unit of odor sampling, yet how sniffing shapes odor representations remains poorly understood. Perhaps the earliest hypothesis of the role of sniffing in olfaction arises from the fact that odorants with different physicochemical properties exhibit different patterns of deposition across the olfactory epithelium, and that these patterns are differentially affected by flow rate. However, whether sniff flow rates shape odor representations during natural sniffing remains untested, and whether animals make use of odorant sorption-airflow relationships as part of an active odor-sampling strategy remains unclear. We tested these ideas in the intact rat using a threefold approach. First, we asked whether sniff strength shapes odor representations in vivo by imaging from olfactory receptor neuron (ORN) terminals during controlled changes in inhalation flow in the anesthetized rat. Second, we asked whether sniff strength shapes odor representations by imaging from ORNs during natural sniffing in the awake rat. Third, we asked whether rats actively modulate sniff strength during an odor discrimination task. We found that, while artificial changes in flow rate can alter ORN responses, sniff strength has negligible effect on odor representations during natural sniffing, and behaving rats do not modulate flow rate to improve odor discrimination. These data suggest that modulating sniff strength does not shape odor representations sufficiently to be part of a strategy for active odor sensing in the behaving animal.

Specific entrainment of mitral cells during gamma oscillation in the rat olfactory bulb.

Local field potential (LFP) oscillations are often accompanied by synchronization of activity within a widespread cerebral area. Thus, the LFP and neuronal coherence appear to be the result of a common mechanism that underlies neuronal assembly formation. We used the olfactory bulb as a model to investigate: (1) the extent to which unitary dynamics and LFP oscillations can be correlated and (2) the precision with which a model of the hypothesized underlying mechanisms can accurately explain the experimental data. For this purpose, we analyzed simultaneous recordings of mitral cell (MC) activity and LFPs in anesthetized and freely breathing rats in response to odorant stimulation. Spike trains were found to be phase-locked to the gamma oscillation at specific firing rates and to form odor-specific temporal patterns. The use of a conductance-based MC model driven by an approximately balanced excitatory-inhibitory input conductance and a relatively small inhibitory conductance that oscillated at the gamma frequency allowed us to provide one explanation of the experimental data via a mode-locking mechanism. This work sheds light on the way network and intrinsic MC properties participate in the locking of MCs to the gamma oscillation in a realistic physiological context and may result in a particular time-locked assembly. Finally, we discuss how a self-synchronization process with such entrainment properties can explain, under experimental conditions: (1) why the gamma bursts emerge transiently with a maximal amplitude position relative to the stimulus time course; (2) why the oscillations are prominent at a specific gamma frequency; and (3) why the oscillation amplitude depends on specific stimulus properties. We also discuss information processing and functional consequences derived from this mechanism.

Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb.

A growing body of data suggests that information coding can be achieved not only by varying neuronal firing rate, but also by varying spike timing relative to network oscillations. In the olfactory bulb (OB) of a freely breathing anaesthetized mammal, odorant stimulation induces prominent oscillatory local field potential (LFP) activity in the beta (10-35 Hz) and gamma (40-80 Hz) ranges, which alternate during a respiratory cycle. At the same time, mitral/tufted (M/T) cells display respiration-modulated spiking patterns. Using simultaneous recordings of M/T unitary activities and LFP activity, we conducted an analysis of the temporal relationships between M/T cell spiking activity and both OB beta and gamma oscillations. We observed that M/T cells display a respiratory pattern that pre-tunes instantaneous frequencies to a gamma or beta regime. Consequently, M/T cell spikes become phase-locked to either gamma or beta LFP oscillations according to their frequency range and respiratory pattern. Our results suggest that slow respiratory dynamics pre-tune M/T cells to a preferential fast rhythm (beta or gamma) such that a spike-LFP coupling might occur when units and oscillation frequencies are in a compatible range. This double-coupling process might define two complementary beta- and gamma-neuronal assemblies along the course of a respiratory cycle.

Odor vapor pressure and quality modulate local field potential oscillatory patterns in the olfactory bulb of the anesthetized rat.

A central question in chemical senses is the way that odorant molecules are represented in the brain. To date, many studies, when taken together, suggest that structural features of the molecules are represented through a spatio-temporal pattern of activation in the olfactory bulb (OB), in both glomerular and mitral cell layers. Mitral/tufted cells interact with a large population of inhibitory interneurons resulting in a temporal patterning of bulbar local field potential (LFP) activity. We investigated the possibility that molecular features could determine the temporal pattern of LFP oscillatory activity in the OB. For this purpose, we recorded the LFPs in the OB of urethane-anesthetized, freely breathing rats in response to series of aliphatic odorants varying subtly in carbon-chain length or functional group. In concordance with our previous reports, we found that odors evoked oscillatory activity in the LFP signal in both the beta and gamma frequency bands. Analysis of LFP oscillations revealed that, although molecular features have almost no influence on the intrinsic characteristics of LFP oscillations, they influence the temporal patterning of bulbar oscillations. Alcohol family odors rarely evoke gamma oscillations, whereas ester family odors rather induce oscillatory patterns showing beta/gamma alternation. Moreover, for molecules with the same functional group, the probability of gamma occurrence is correlated to the vapor pressure of the odor. The significance of the relation between odorant features and oscillatory regimes along with their functional relevance are discussed.

A wavelet-based method for local phase extraction from a multi-frequency oscillatory signal.

One of the challenges in analyzing neuronal activity is to correlate discrete signal, such as action potentials with a signal having a continuous waveform such as oscillating local field potentials (LFPs). Studies in several systems have shown that some aspects of information coding involve characteristics that intertwine both signals. An action potential is a fast transitory phenomenon that occurs at high frequencies whereas a LFP is a low frequency phenomenon. The study of correlations between these signals requires a good estimation of both instantaneous phase and instantaneous frequency. To extract the instantaneous phase, common techniques rely on the Hilbert transform performed on a filtered signal, which discards temporal information. Therefore, time-frequency methods are best fitted for non-stationary signals, since they preserve both time and frequency information. We propose a new algorithmic procedure that uses wavelet transform and ridge extraction for signals that contain one or more oscillatory frequencies and whose oscillatory frequencies may shift as a function of time. This procedure provides estimates of phase, frequency and temporal features. It can be automated, produces manageable amounts of data and allows human supervision. Because of such advantages, this method is particularly suitable for analyzing synchronization between LFPs and unitary events.

Respiratory cycle as time basis: an improved method for averaging olfactory neural events.

In the mammalian olfactory system, neural activity appears largely modulated by respiration. Accurate analysis of respiratory synchronized activity is precluded by the variability of the respiratory frequency from trial to trial. Thus, the use of respiratory cycle as the time basis for measuring cell responses was developed about 20 years ago. Nevertheless, averaging oscillatory component of the activity remains a challenge due to their rhythmic features. In this paper, we present a new respiratory monitoring setup based on the measurement of micropressure changes induced by nasal airflow in front of the nostril. Improvements provided by this new monitoring setup allows automatic processing of respiratory signals in order to extract each respiratory period (expiration and inspiration). The time component of these periods, which can differ from trial to trial, is converted into a phase component defined as [-pi, 0] and [0, pi] for inspiration and expiration, respectively. As opposed to time representation, the phase representation is common to all trials. Thus, this phase representation of the respiratory cycle is used as a normalized time basis permitting to collect results in a standardized data format across different animals and providing new tools to average oscillatory components of the activity.