134 Biochemical Society Transactions (2003) Volume 31, part 1

Grouping of odorant receptors: odour maps in the

mammalian olfactory bulb
K. Mori1
Department of Physiology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113–0033, Japan

Abstract
The olfactory system is unique in that the sensory input is in the form of molecular information carried in a vast
variety of odorants. Nearly 1000 types of odorant receptors mediate the initial detection and discrimination
of odorants at the molecular-feature level. The discrimination at the molecular level is converted into that at
the cellular level (olfactory sensory neurons) by the one sensory neuron–one odorant receptor rule, and then
into that at the neuronal circuit level in the olfactory bulb by the specific olfactory axon connectivity pattern.
Individual glomeruli in the olfactory bulb represent a single odorant receptor, and the glomerular sheet at
the olfactory bulb surface forms odorant receptor maps. This review focuses on the spatial organization of the
glomerular sensory map in the olfactory bulb. The analysis using the optical imaging method suggests that
odorant receptors having a common molecular-feature receptive site are grouped together and represented
by glomeruli that are localized in topographically fixed domains in the olfactory bulb. The domain organization
may be a structural unit for the spatial organization of the glomerular sensory map, and might relate to the
olfactory submodality.

Introduction odorant receptors mediate the initial detection and discrimi-

Olfactory signalling plays a key role in a variety of animal
behaviours such as territorial marking, food-, predator-
and kin-recognition and sexual behaviour. In mammals, the
chemical signal typically consists of a complex mixture of
dozens of different odour molecules or odorants. Odorants
are small volatile compounds with molecular masses of
approx. 25–300 Da. It has been estimated that more than
400 000 different compounds are odorous to the human nose.
Thus, the major task of the olfactory nervous system is to
detect and discriminate an immense variety of odorants, as
well as to process and integrate the molecular information
carried by a complex mixture of odorants for identifying
a specific object. Recent studies using multidisciplinary
approaches have begun to reveal the logic employed by the
olfactory nervous system for the discrimination of numerous
odorants at the molecular, cellular and neuronal circuit levels
[1–4].
To cope with a huge variety of odorants, mammals
have developed nearly 1000 types of odorant receptors [5].
Odorant receptors are 7-transmembrane G-protein-coupled
membrane proteins that are expressed on the cilia of olfactory
sensory neurons in the nasal olfactory epithelium. Each
odorant receptor presumably detects distinct molecular
structures/features of odorants, and thus binds to a specific
range of odorants that share the molecular structures/features
[6–8]. Each odorant can bind to multiple, but specific, odorant
receptors. Thus, the binding between ligand odorants and
odorant receptors shows a complex multiple-to-multiple, not
a simple one-to-one, relationship. The approx. 1000 types of
Key words: glomerulus, molecular-feature domain, olfactory sensory map.
1
e-mail moriken@m.u-tokyo.ac.jp
nation of the molecular features of odorants. To discriminate
among numerous odorants or complex mixtures of odorants,
the brain needs to know which combination of odorant re-
ceptors is activated by the inhaled odorants.
The logic of discrimination at the molecular level is
converted into that at the cellular level (olfactory sensory
neurons) by one sensory neuron – the one odorant receptor
rule. Individual sensory neurons express only a single type of
odorant receptor among a repertoire of approx. 1000 [2,4,7,9].
The information at the cellular level is further converted into
that at the neuronal circuit level by a specific connectivity
pattern of olfactory axons. Olfactory sensory neurons
expressing a given type of odorant receptor are scattered
widely in the olfactory epithelium, but their axons converge
onto a few fixed glomeruli in the olfactory bulb, the first
centre for the processing of odorant information [10–13].
Furthermore, individual glomeruli presumably represent a
single type (or at most a few types) of odorant receptor(s).
Therefore, to determine which of the numerous odorant
receptors have been activated by the inhaled odorants, the
brain only needs to examine which combination of glomeruli
has been activated.
Glomerular sensory map in the olfactory
bulb
Glomeruli are spherical neuropils within which olfactory
axons form excitatory synaptic terminals on the primary
dendrites of mitral and tufted cells, the principal neurons in
the olfactory bulb [14]. Individual mitral/tufted cells project
a single primary dendrite to a single glomerulus, and thus
receive excitatory inputs selectively from olfactory axons that

C 2003 Biochemical Society

originate from sensory neurons that express a given odorant
receptor.
In mice, an individual olfactory bulb contains approx. 1800
glomeruli. If we refer to a glomerulus with its associated
neurons as a glomerular module, the architecture of the
mouse olfactory bulb can be simplified by being composed
of approx. 1800 such modules. The physical arrangement of
the glomerular modules indicates the presence of an odor-
ant receptor map in the olfactory bulb. How is the odorant
receptor map spatially arranged in the olfactory bulb? I
would like to review an emerging view regarding the spatial
organization of the olfactory sensory map in the mammalian
olfactory bulb.
For a majority of odorant receptors, individual receptors
are expressed by sensory neurons that are distributed widely
in one of the four zones (I, II, III, and IV) of the
olfactory epithelium [15–17]. In mice, each of the zone-
specific odorant receptors is usually represented by two
glomeruli, one in the lateral and the other in the medial part
of the olfactory bulb [10,18]. The plotting of the position of
glomeruli representing the zone-specific odorant receptors,
together with the knowledge of the zonal arrangement of
glomeruli in the olfactory bulb [19] suggests that each
olfactory bulb contains two mirror-image sensory maps of
zone-specific odorant receptors [20]. One map is located
in the rostrolateral hemisphere, and the other map in the
caudomedial hemisphere of the olfactory bulb.
A small group of odorant receptors do not show a zone-
specific expression pattern in the olfactory epithelium, and are
expressed by sensory neurons that are clustered densely in a
specific part of the olfactory epithelium [21]. An individual
odorant receptor of this group is typically represented by a
single glomerulus that is located at the most ventral portion
of the olfactory bulb [22]. Thus, each olfactory bulb contains
two symmetrical sensory maps, which represent the large
group of zone-specific odorant receptors and a small map
at the most ventral part representing the non-zonal odorant
receptors.
Odorant response map in the olfactory bulb
Analyses of the spatial mapping of odorant-induced activity
in the mammalian olfactory bulb have been reported
with several different types of methods. The mapping
methods include optical imaging of intrinsic signals [23–26],
2-deoxyglucose uptake [27–32], electrophysiological record-
ing of single neuron activity [13] and expression of immedi-
ate early genes such as c-fos, and zif268 [33–37]. These studies
show that each odorant elicits a characteristic spatial pattern
of activity in the olfactory bulb. The mapping studies with
2-deoxyglucose uptake or immediately early genes [29–32,37]
show that the odorant-induced activity is localized in a
symmetrical fashion in accord with the symmetrical maps of
zone-specific odorant receptors.
The method of optical imaging of intrinsic signals enables
us to map the responses to many different odorants in the
same olfactory bulb with a relatively high spatial resolution
Signalling the Future 135
at a single-glomerulus level [23]. By using this method,
we demonstrated that the dorsal surface of the olfactory
bulb contained at least two molecular-feature domains, the
anteromedial domain and the lateral domain, at stereotypical
positions [24]. Glomeruli within each domain respond
selectively to specific ranges of odorants. Homologous series
of fatty acids, aliphatic aldehydes, and a subset of esters acti-
vate glomeruli that are clustered in the anteromedial do-
main, whereas aliphatic alcohols, phenols, ketones, and
a different subset of esters activate glomeruli in the lateral
domain.
Detailed analysis of the spatial position of odorant-
activated glomeruli in terms of the two molecular-feature
domains indicates that the molecular features of odorants
can be categorized into two classes, primary features and
secondary features, which differentially affect the odorant-
evoked activity in the glomerular sensory map. Primary
features are molecular profiles that characterize each domain.
For the two domains, the primary features are functional
groups and their position in the molecule. Secondary
features are molecular profiles that are represented by local
arrangement of glomeruli within each domain. In the two
domains, the secondary features include the length and
branching pattern of carbon chains. In addition, the antero-
medial domain has a polarity such that the systematic
and gradual shift of the positions of activated glomeruli
occurs with the increase in the carbon-chain length of
odorant.
Similar molecular-feature domains are present in many
parts of the olfactory bulb [31,37]. The molecular-feature
domains might be a structural unit for the spatial organization
of the glomerular sensory map. The presence of molecular-
feature domains suggests that odorant receptors having a
common or similar molecular feature receptive site are
grouped together and represented by glomeruli within each
domain.
A number of psychophysical studies have shown a close
relationship between the molecular features/structures of
odorants and our subjectively perceived ‘odour’. For example,
functional groups of odorants such as –COOH and –OH
strongly influence odour quality. Therefore, the finding of
molecular-feature domains and the domain-specific grouping
and representation of specific subsets of odorant receptors
raises an interesting possibility that the specific group of
glomerular modules in each molecular-feature domain might
relate to an olfactory submodality or a major quality of
subjectively perceived ‘odour’. Further studies are needed
to examine the above possibility, as well as to address the
question of how the odorant receptor maps in the olfactory
bulb are transformed to functional sensory maps in various
regions of the olfactory cortex, which are the target regions
of the mitral/tufted cell axons.
This work was supported by Grant-in-Aid for Creative Scientific
Research from the Japan Society for the Promotion of Science.


C 2003 Biochemical Society
136 Biochemical Society Transactions (2003) Volume 31, part 1
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Received 6 September 2002