Olfactory maps and odor images

doi:10.1016/S0959-4388(02)00348-3

Current Opinion in Neurobiology

Volume 12, Issue 4, 1 August 2002, Pages 387-392

https://doi.org/10.1016/S0959-4388(02)00348-3 Get rights and content

Abstract

The understanding of neuronal processing of olfactory stimuli has been furthered by genetic studies and specialized imaging of particular neuronal populations. Selective optical imaging of odor-induced presynaptic and postsynaptic glomerular activity in the olfactory bulb/antennal lobe has visualized odorant-responsive receptor repertoires and shown a more confined odor image at the level of projection neurons compared to their olfactory receptor neuron input. Genetic tracing of projection neurons connected to particular glomeruli has revealed a somewhat dispersed spatial map of termination areas for these neurons both in insects and in vertebrates. Modifications of the glomerular odor map have resulted in altered percepts of the corresponding odors.

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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Whilst the senses of vision and hearing have been successfully automated and miniaturized in portable formats (e.g. smart phone), this is yet to be achieved with the sense of smell. This is because the sensing challenge is not trivial as it involves navigating a chemosensory space comprising thousands of volatile organic compounds. Distinct aroma recognition is based on detecting unique combinations of volatile organic compounds. In natural olfactory systems this is accomplished by employing odorant receptors (ORs) with varying specificities, together with combinatorial neural coding mechanisms. Attempts to mimic the remarkable sensitivity and accuracy of natural olfactory systems has therefore been challenging. Current portable chemical sensors for odorant detection are neither sensitive nor selective, prompting research exploring artificial olfactory devices that use natural OR proteins for sensing. Much research activity to develop OR based biosensors has concentrated on mammalian ORs, however, insect ORs have not been explored as extensively. Insects possess an extraordinary sense of smell due to a repertoire of odorant receptors evolved to interpret olfactory cues vital to the insects' survival. The potential of insect ORs as sensing elements is only now being unlocked through recent research efforts to understand their structure, ligand binding mechanisms and development of odorant biosensors. Like their mammalian counterparts, there are many challenges with working with insect ORs. These include expression, purification and presentation of the insect OR in a stable display format compatible with an effective transduction methodology while maintaining OR structure and function. Despite these challenges, significant progress has been demonstrated in developing OR-based biosensors which exploit insect ORs in cells, lipid bilayers, liposomes and nanodisc formats. Ultrasensitive and highly selective detection of volatile organic compounds has been validated by coupling these insect OR display formats with transduction methodologies spanning optical (fluorescence) and electrical (field effect transistors, electrochemical impedance spectroscopy) techniques. This review summarizes the current status of insect OR based biosensors and their future outlook.
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Studies on Kenyon Cells (KCs) in the olfactory system of locust have found evidence that some of them are more responsive towards stimuli than others. This variability suggests that there could be a heterogeneous neural threshold distribution among KCs. This work explores the hypothesis that the heterogeneity in neural thresholds could control the activity level of populations of neurons and facilitate the generation of sparse code to achieve a better representation of stimuli. In order to study this hypothesis, an artificial neural network that adapts many of the strategies observed in the locust olfactory system is proposed, including a new learning algorithm capable of finding the best neural threshold distribution to resolve a certain classification problem and a gain control term that keeps the activity level of the neurons in the hidden layer under a certain limit. The bio-inspired neural network gets the best results when the activity level in the hidden layer is low, for which neural thresholds are more important for a better performance than the connections between the neurons in different layers. Also, it was found that the separability of the internal representations of the different patterns in the classification problem improves when the thresholds are adjusted by the learning algorithm in order to control the activity level. Finally, the performance of this network was compared to SVMs and MLP when applied to resolve a complex classification task with data collected by electronic noses and affected by sensor drift, for which the bio-inspired network obtains very satisfactory results, reaching a performance similar or even better than SVMs and MLP.
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Olfactory receptors mediate the primary interaction of the olfactory brain with the external world. Any odor stimulus is initially represented as activation of one to many different olfactory receptors. Vice versa, anything that binds and activates an olfactory receptor is as per definition an odor, or odorant, as the single compounds are often called. Olfactory receptors constitute one of the largest families of G-protein-coupled receptors. Many large and small clusters of olfactory receptors are distributed throughout the genome. Olfactory receptors are expressed in a highly specific manner and monogenic expression is the general rule, that is, one neuron–one receptor. The molecular receptive range has been analyzed for several olfactory receptors. Generally, olfactory receptors have been found to exhibit a somewhat relaxed specificity toward ligands. However, some receptors, in particular, those for pheromones, show very high specificity. Olfactory receptors signal through specialized trimeric G proteins to open calcium-permeable nonspecific cation channels.
Interaction between cAMP and intracellular Ca<sup>2 +</sup>-signaling pathways during odor-perception and adaptation in Drosophila
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Citation Excerpt :
Insect ORs serves both as odorant receptors and as ion channels [24,25] and thus, in insects, both metabotropic and ionotropic signaling mediate odor-transduction at ORNs [24,26]. Nevertheless, despite these fundamental differences in transduction machineries, the odor coding strategy at ORNs remains similar between insects and mammals [27–33]. Transduction mechanism at ORNs is mediated by cAMP and/or InsP3-signaling pathways in an odorant-dependent manner [34].
Binding of an odorant to olfactory receptors triggers cascades of second messenger systems in olfactory receptor neurons (ORNs). Biochemical studies indicate that the transduction mechanism at ORNs is mediated by cyclic adenosine monophosphate (cAMP) and/or inositol,1,4,5-triphosphate (InsP3)-signaling pathways in an odorant-dependent manner. However, the interaction between these two second messenger systems during olfactory perception or adaptation processes is much less understood. Here, we used interfering-RNAi to disrupt the level of cAMP alone or in combination with the InsP3-signaling pathway cellular targets, InsP3 receptor (InsP₃R) or ryanodine receptor (RyR) in ORNs, and quantify at ORN axon terminals in the antennal lobe, the odor-induced Ca²⁺-response. In-vivo functional bioluminescence Ca²⁺-imaging indicates that a single 5 s application of an odor increased Ca^2 +-transients at ORN axon terminals. However, compared to wild-type controls, the magnitude and duration of ORN Ca^2 +-response was significantly diminished in cAMP-defective flies. In a behavioral assay, perception of odorants was defective in flies with a disrupted cAMP level suggesting that the ability of flies to correctly detect an odor depends on cAMP. Simultaneous disruption of cAMP level and InsP₃R or RyR further diminished the magnitude and duration of ORN response to odorants and affected the flies' ability to detect an odor. In conclusion, this study provides functional evidence that cAMP and InsP3-signaling pathways act in synergy to mediate odor processing within the ORN axon terminals, which is encoded in the magnitude and duration of ORN response.
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ReviewOlfactory maps and odor images

Abstract

Introduction

Section snippets

Odorant receptors are mainly oligo-specific

From randomness to order in one step

Development of the glomerular map

The odor image in the olfactory bulb

Presynaptic versus postsynaptic odor map in the olfactory bulb

Olfactory maps in higher olfactory centers

Odor images within higher olfactory centers

Conclusions

References and recommended reading

Cell

Neuron

Cell

Cell

Neuron

Cell

Curr Biol

Cell

Neuron

Neuron

Neuron

Neuron

Neuron

Cell

Cell

Neuron

Chemosensory signaling in C. elegans

Bioessays

The molecular logic of olfaction in Drosophila

Chem Senses

Different evolutionary processes shaped the mouse and human olfactory receptor gene families

Hum Mol Genet

Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors

Nat Neurosci

Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ

J Neurosci

Guanylyl cyclases as a family of putative odorant receptors

Annu Rev Neurosci

Neuropharmacology. Odorants may arouse instinctive behaviours

Nature

How the olfactory system makes sense of scents

Nature

Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants

J Neurosci

Peripheral mechanisms of pheromone reception in moths

Chem Senses

Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer

J Neurosci

Ultrasensitive pheromone detection by mammalian vomeronasal neurons

Nature

A photoaffinity-labeled green leaf volatile compound ‘tricks’ highly selective and sensitive insect olfactory receptor neurons

Chem Senses

Functional analysis of an olfactory receptor in Drosophila melanogaster

Proc Natl Acad Sci USA

Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system

Proc Natl Acad Sci USA

A single olfactory receptor specifically binds a set of odorant molecules

Eur J Neurosci

Odorant receptor expression defines functional units in the mouse olfactory system

J Neurosci

Odorant feature detection: activity mapping of structure response relationships in the zebrafish olfactory bulb

J Neurosci

Expression of mRNAs encoding for two different olfactory receptors in a subset of olfactory receptor neurons

J Neurochem

Zonal organization of the mammalian main and accessory olfactory systems

Philos Trans R Soc Lond B Biol Sci

Nested expression domains for odorant receptors in zebrafish olfactory epithelium

Proc Natl Acad Sci USA

Chemical determinants of the rat electro-olfactogram

J Neurosci

A role for the EphA family in the topographic targeting of vomeronasal axons

Development

Review
Olfactory maps and odor images