What do electrophysiological studies tell us about processing at the olfactory bulb level?

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Abstract

Electrophysiological recordings performed in the mammalian olfactory bulb (OB) aimed at deciphering neural rules supporting neural representation of odors. In spite of a fairly large number of available data, no clear picture emerges yet in the mammalian OB. This paper summarizes some important findings and underlines the fact that difference in experimental conditions still represents a major limitation to the emergence of a synthetic view. More specifically, we examine to what extent the absence or the presence of anaesthetic influence OB neuronal responsiveness. In addition, we will see that recordings of either single cell activity or populational activity provide quite different pictures. As a result some experimental approaches provide data underlying sensory properties of OB neurons while others emphasize their capabilities of integrating incoming sensory information with attention, motivation and previous experience.

Introduction

In sensory physiology, primary neocortical sensory areas are defined as those receiving their input from their specific thalamic relay. This is not the case in the olfactory system in which olfactory information reaches thalamic areas after it has been processed in the olfactory bulb and the piriform cortex. Consequently, primary olfactory area cannot be defined from its connectivity. In mammals, primary olfactory receptors in the nasal cavities send their axon to an ovoid like structure, the olfactory bulb. This primitive cortical area is an obvious candidate as the primary olfactory cortex. Output cells of the olfactory bulb (mitral and tufted cells) send their axons to the widespread piriform cortex in the ventral surface of the rodent’s brain. Anatomists mostly consider this area as the primary olfactory cortex (Wilson and Mainen, 2006). In this perspective, how should olfactory bulb be classified? Since there is no strict anatomical criterion for defining primary and secondary olfactory cortices one should consider their functional characteristics. From this point of view, primary cortical areas should contain output cells responding with high reproducibility to specific simple features of the stimulus and secondary areas to more complex features. For example, pyramidal cells of the primary visual and auditory areas respond to bars of a specific orientation and tones in a narrow frequency band, respectively. Secondary visual and auditory cortices are found to respond to more complex stimuli such object categories and voices. In the olfactory system, experimental demonstration of an analogous functional difference between olfactory bulb and piriform cortex would help in defining which one can be defined as the primary area. Electrophysiological recordings represent the main tool for investigating this question. Importantly, the vast majority of available data has been collected at the olfactory bulb level and much less is known at the piriform cortex level (Wilson, 2001). Due to their position in olfactory pathways and to their intrinsic organization, olfactory bulb output neurons are suspected to “extract” fundamental dimensions of the olfactory stimulus while piriform cortex plays role both in features extraction and associative memory (Haberly, 2001, Hasselmo and Bower, 1989, Litaudon et al., 1997, Mouly et al., 2001). In this paper we will focus on some sets of electrophysiolgical experiments aimed at identifying major functional characteristic of OB relay neurons. A good understanding of OB processing is a prerequisite for interpretation of computation at the piriform cortex level. This paper is not aimed at reviewing the whole set of available data. The main purpose is to emphasize the difficulty in integrating data collected in different experimental conditions. More specifically, we will underline the importance of two major variables: the first one is whether recordings were obtained in awake freely moving rat or from anesthetized animals. The second one is whether single cells or populational recordings were performed. As it is the case for other cortical areas, neural responsiveness has mainly been investigated through single cell recordings. Apart from the pioneer works performed by Adrian in the forties (Adrian, 1950) and later on by Freeman (Freeman, 1978, Freeman and Schneider, 1982), much less attention has been paid to populational activity collected by macroelectrodes. This type of activity can be obtained from surface electrodes (EEG) or from deeply implanted electrodes (local field potential). We will see that on one hand, data from single cells recordings in anesthetized animals reveal OB responsiveness partly compatible to the one expected from a primary sensory areas. On the other hand, data obtained from EEG, LFP recordings and single cells activity in awake behaving animals show a much more complex picture revealing characteristic found in secondary cortical areas. In addition, we will see that electrophysiological correlates of odor quality are still elusive.

Section snippets

Different recordings conditions determine the way OB is considered

In intact mammals electrophysiolgical recordings are obtained either under anesthesia or in the absence of anesthesia in restrained or freely behaving animals. These two approaches have been applied extensively in the rodent olfactory bulb. Importantly, one has to point that both spontaneous and odor-induced activity recorded in each condition are determined differently. In anesthetized animals, OB responsivess is primarily if not solely dependent on the nature of the odorant presented in front

Some behavioral considerations

Considering that the purpose of electrophysiological studies is to decipher at least some neural correlates of odorant discrimination, these correlates would have to present a temporal dynamic compatible to the time required by animals to discriminate odors. In rodents, this question has been addressed recently by several authors (Uchida and Mainen, 2003, Abraham et al., 2004, Rinberg et al., 2006b, Ravel et al., 2003, Martin et al., 2004, Martin et al., 2006). In these behavioral experiments

Some neural correlates of odor representation as seen at the single unit level

Under anesthesia, a large number of experiments examined single cell (presumably mitral or tufted cells) responsiveness to odorant presentation (Buonviso et al., 2003, Chaput et al., 1992). Detailed description of such set of data can be found elsewhere (Ache and Young, 2005, Lledo et al., 2005). Here we point out some general features. First, it is worth to note that in these experiments odorants presentations are at relatively high concentration and lasted for several seconds (5–10 sec). One

Some neural correlates of odor representation as seen at the populational level

It is well established that olfactory structures together with limbic ones developed prominent populational oscillatory activities. This was found first at the OB level in the late forties in anesthetised hedgehog (Adrian, 1950) and described in detail later in awake restrained rabbits (Freeman, 1978). When macrolectrodes (80–100 m diameter) are positioned at the surface of the OB or deep in the structure, clear-cut oscillatory regimes are detected. Surface recordings are EEGs and deeper ones

Concluding remarks

As already pointed out (Rinberg et al., 2006a, Rinberg and Gelperin, 2006), electrophysiological correlates of neural representation at the OB level markedly differed according to two major variables: anaesthesia vs awake behaving animals and the type of recordings (single cell vs populational). Data obtained in these different conditions are hardly reconcilable. This difficulty emerges for at least two reasons. First, at the OB level, each odorant seems so to be represented by widespread

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