Review
Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb

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Abstract

Input from olfactory receptor neurons is first organized and processed in the glomerular layer of the olfactory bulb. Olfactory glomeruli serve as functional units in coding olfactory information and contain a complex network of synaptic connections. Odor information has long been thought to be represented by spatial patterns of glomerular activation; recent work has, additionally, shown that these patterns are temporally dynamic. At the same time, recent advances in our understanding of the glomerular network suggest that glomerular processing serves to temporally sharpen these dynamics and to modulate spatial patterns of glomerular activity. We speculate that odor representations and their postsynaptic processing are tuned to and shaped by the sniffing behavior of the animal.

Introduction

Olfactory glomeruli constitute the first stage of synaptic processing of olfactory information. Glomeruli themselves are discrete anatomical structures whose presence and general organization is remarkably well conserved across species and even phyla [1], [2], [3], [4]. Olfactory glomeruli have long been hypothesized to play a critical role in odor coding. Only recently, however, has an integrated picture emerged of the molecular, anatomical and functional relationship between olfactory glomeruli, the olfactory receptor neurons (ORNs) which project to them, and their representation of olfactory information. At the same time, recent studies have shed new light on the complexity of the synaptic network in the glomerular layer and the various roles this network plays in processing olfactory input. This review focuses on strategies for representing and processing olfactory information in terms of activity in and among olfactory glomeruli. We place special emphasis here on the role of temporally dynamic activity patterns in the glomerular layer, whose role in odor coding and processing is becoming increasingly recognized. Several excellent reviews provide more detailed descriptions of olfactory coding in terms of static activity patterns [5], [6], [7].

Section snippets

Glomeruli as anatomical and functional units

The projection of receptor neurons to olfactory glomeruli forms the first transformation of odorant-evoked activity patterns in the nervous system. This projection is massively convergent, with (on average) several thousand ORNs converging onto each glomerulus of the mammalian olfactory bulb [8], [9]. Each of the several thousand ORNs expressing the same OR converge onto one, two or a few glomeruli in the olfactory bulb [10], [11], [12]. Typically, each OR-expressing population of ORNs targets

Intrinsic and synaptic properties of juxtaglomerular neurons

The spatial and temporal characteristics of glomerular activity maps discussed to this point are the results of properties inherent in ORNs and the “rules” governing their glomerular targeting. These characteristics neither involve nor require interactions among ORNs. Upon synapsing in the glomerulus, ORNs release glutamate [67] and engage postsynaptic mechanisms that initiate the neural processing of olfactory input. From this point on, neural processing involves not only the intrinsic

Presynaptic inhibition of ORN input to glomeruli

One glomerular processing pathway that has been extensively characterized is that mediating presynaptic inhibition of transmitter release from ORNs. Feedback from glomerular interneurons onto ORN axon terminals suppresses transmitter release in mammals [93], [94], [95], reptiles [96] and arthropods [97]. In each species, multiple synaptic pathways work in parallel to modulate ORN input. In glomeruli of the mammalian OB, both GABA- and dopaminergic pathways are involved in presynaptic

Role of glomerular processing in shaping odor representations in vivo

How might the presynaptic and postsynaptic glomerular network function together to shape spatial and temporal patterns of activity as olfactory input is transmitted from ORNs to MT cells? We speculate that this network is optimally organized to impose brief temporal windows over which MT cells can be excited by rhythmic ORN inputs, while at the same time maintaining responsiveness across a wide range of input strengths. We further speculate that spatial patterns of MT activity are sharpened via

Acknowledgments

The authors would like to thank A. Puche for critical comments on the manuscript and assistance with the figures. Work in the authors’ laboratories is supported by grants from the National Institutes of Health.

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