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