ReviewOlfactory maps and odor images
Introduction
When the brain extracts olfactory information from an odor stimulus, it performs a multi-level task. At each level of neuronal processing, a modified representation of the odor stimulus is generated, as specified by the particular mapping function for that level (Fig. 1). The odor map thus generated may be a straightforward spatial map, but it can also be a spatiotemporal map or even a map in virtual space. To understand the logic of olfactory information processing, we will have to appreciate the odor maps generated at each level, from the odorant receptors up to the level of the olfactory cortex. Both anatomical olfactory maps and functional activity maps (odor images) are instructive in this respect. In this review, I restrict myself to a discussion of vertebrate and insect olfactory systems, between which considerable similarities in the molecular logic of olfaction have been demonstrated. However, it should be noted that different strategies may be used in other phyla [1].
Section snippets
Odorant receptors are mainly oligo-specific
The outline of the olfactory information-processing pathway is schematically represented in Fig. 1. Information processing begins with the mapping of an odor or odorant — a single odorous substance — to the subset of odorant receptors that it activates. This odor map or odor image might be considered a map in receptor space. The tuning properties of the individual odorant receptors will determine the properties of the odor image at this level.
Two large families of odorant receptors have been
From randomness to order in one step
Due to the one receptor–one receptor neuron relationship, the odor map in receptor space translates directly to a map of activated ORNs. Receptor neurons are coarsely ordered into several zones (mammals) or domains (fish and insects) depending on the odorant receptor they express 2., 25., 26.. A coarse spatial heterogeneity of odor responses within the sensory surface in both vertebrates [27] and insects [24•] reflects this loose organization, as does the zonal distribution of several axon
Development of the glomerular map
The convergence of like axons from scattered olfactory somata onto a common glomerulus poses a major pathfinding problem during the development and regeneration of ORNs (reviewed in 25., 31.). The past year has provided some detailed morphological studies that show that axons target glomeruli very precisely and that glomeruli, in turn, receive very homogeneous input with regard to the OR expressed by the innervating ORNs [39•]. A developmental study of radial glia processes suggests that these
The odor image in the olfactory bulb
Imaging odor-induced activity in the olfactory bulb or antennal lobe has identified the combinatorial activation of several glomeruli by individual odorants (reviewed in 30., 47.), consistent with the kind of tuning properties observed for some individual odorant receptors (see above). Several analysis methods — 2-deoxyglucose uptake 48., 49., intrinsic signals ([50] and references cited therein), calcium indicators [51] and voltage-dependent dyes 13., 52. — have yielded rather consistent
Presynaptic versus postsynaptic odor map in the olfactory bulb
The presynaptic signal in glomeruli may be determined separately from the postsynaptic component by selectively labeling ORNs with a calcium indicator dye [51]. Such measurements have been performed in the zebrafish olfactory bulb [51] and subsequently in mammals 53•., 60•.; these results are generally similar to those of summary determinations of presynaptic and postsynaptic signal components in the olfactory bulb 47., 48., 49., 50..
Direct comparison of mitral cell responses with the
Olfactory maps in higher olfactory centers
Traditionally, controversy has surrounded the extent to which projection neurons emanating from the olfactory bulb retain spatial patterning in their termination fields in the second relay station, the higher olfactory brain centers (piriform cortex, anterior olfactory nucleus, olfactory tubercle and entorhinal cortex in mammals; mushroom body and protocerebrum in insects). However, in species where the axons of projection neurons leave the olfactory bulb in more than one tract, generally,
Odor images within higher olfactory centers
The olfactory maps embodied by distinct clusters of pyramidal neurons connected indirectly to like receptor neurons [73••] may not be reflected in the cortical activity maps elicited by particular odors. Second order projection neurons (pyramidal cells) receiving input from mitral cells connect to a multitude of neurons both within the piriform cortex and outside it, and neighboring pyramidal cells generally exhibit disparate projection patterns 77., 78.. Optical imaging of higher olfactory
Conclusions
Our understanding of the neuronal processing of olfactory stimuli has been furthered by genetic manipulations and specialized imaging of particular neuronal populations. The cortical termination areas of projection neurons connected to individual glomeruli are stereotyped and distinct, albeit overlapping, in contrast to their dendritic fields, which are segregated. Such an overlap may enable crosstalk between different information strands. Selective imaging of odor-induced presynaptic
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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