Chem. Senses 28: 269-278,
2003
© Oxford University Press 2003
Dose–Response Characteristics of Glomerular Activity in the Moth Antennal Lobe
Department of Crop Science, Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
Correspondence to be sent to: Bill S. Hansson, Department of Crop Science, Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden. e-mail: bill.hansson{at}vv.slu.se
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Abstract |
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Odours are represented as unique combinations of activated glomeruli in the antennal lobes of insects. Receptor neurons arborizing in the glomeruli are not only qualitatively selective, but in addition respond to variations in stimulus concentration. As each glomerulus likely represents a single receptor neuron type, optical recordings of calcium changes in insect antennal lobes show how concentration variations affect a large population of afferents. We measured the glomerular responses in the moth Spodoptera littoralis to different concentrations of plant-related odorants. Localized calcium responses were shown to correspond to individual glomeruli. We found that the dynamic range of glomerular responses spanned 3–4 log units of concentration and the most strongly responding glomeruli often reached a plateau at high stimulus doses. Further, we showed that the single most active glomerulus was often not the same across concentrations. However, if the principal glomerulus moved, it was generally to an adjacent or proximal glomerulus. As concentration increased, a higher number of glomeruli became activated. Correlations of glomerular representations of the same compound at different doses decreased as the difference in concentration increased. Moreover, representations evoked by different odorants were more correlated at high than at low doses, which means that the uniqueness of activity patterns decreased with increasing concentration. Thus, if odours are coded as spatial patterns of glomerular activity, as has been suggested, these olfactory codes are not persistent across concentrations.
Key words: olfaction, Spodoptera littoralis, optical imaging, plant volatile, spatial coding
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The insect olfactory system is not only designed to detect and to discriminate between a vast array of odour molecules, but also to sense changes in stimulus concentration. The molecular density in the environment may vary considerably. For example, low concentrations of flower odours can attract an insect over a long distance. The same insect should also be able to cope with the high concentrations of molecules within the petals of a flower when feeding on nectar, without adapting the system. Olfactory receptor neurons (ORN) respond to increased concentrations by an increase in action potential frequency. A number of studies have shown that insect ORNs respond to molecular concentration changes over several orders of magnitude (Hansson, 1995
;
Todd and Baker, 1999).
In the antennal lobes (AL) of insects or olfactory bulbs of vertebrates,
odours are represented by different combinations of responding glomeruli
(Sharp et al., 1975;
Kauer, 1988;
Rodrigues, 1988;
Cinelli et al., 1995;
Friedrich and Korsching, 1997;
Joerges et al., 1997;
Distler et al., 1998;
Johnson et al., 1998;
Galizia et al., 1999;
Rubin and Katz, 1999;
Uchida et al., 2000;
Meister and Bonhoeffer, 2001;
Carlsson et al.,
2002). Only few studies, however, have paid attention to how
concentration variations affect the odour-evoked representations in the lobe
or bulb. If a glomerular activity pattern represents a spatial olfactory code,
as has been suggested (Johnson et
al., 1998; Galizia et
al., 1999), relative patterns should remain identical at
different concentrations to preserve the qualitative information. If patterns
are not identical, quality perception may vary with concentration. Spatial
coding, however, likely functions either in parallel or in combination with an
olfactory temporal code (Laurent et
al., 2001). Temporal characteristics of output signals in
moth ALs are not only stimulus-specific, but also vary with concentration
(Christensen et al.,
2000). The perception of odour quality has in several instances
been shown to be concentration-dependent. For example, olfactory responses of
the fruit fly Drosophila melanogaster shift from attraction to
repulsion as the concentration increases
(Siddiqi, 1983;
Stensmyr et al.,
2003). Furthermore, a few psychophysical studies in humans have
reported altered qualitative perception of some odours due to changed
concentrations (Gross-Isserof and Lancet,
1988; Arctander,
1994). Glomerular activity patterns in vertebrates, observed in
functional imaging experiments, have proven concentration-dependent, often
with a recruitment of active glomeruli
(Rubin and Katz, 1999;
Johnson and Leon, 2000;
Fuss and Korsching, 2001;
Meister and Bonhoeffer, 2001;
Wachowiak and Cohen, 2001;
Fried et al., 2002).
In the zebra fish, for example, dissimilarity between pairs of activity
patterns, evoked by closely related amino acids, was heavily reduced at high
concentrations (Fuss and Korsching,
2001). Concentration-invariant activity patterns have, however,
also been reported (Joerges et
al., 1997; Johnson and
Leon, 2000; Wachowiak et al.,
2000,
2002).
In a previous Ca2+-imaging study in the moth Spodoptera
littoralis, we demonstrated that different odorants were represented as
unique combinations of activated glomeruli
(Carlsson et al.,
2002). The questions we aim to address in the present study
concern the effect of stimulus concentration on odour representations. We
investigate the persistence of glomerular activity across a range of
concentrations with respect to location of activity focus, number of activated
glomeruli and correlation of patterns at different concentrations. Another
imaging study in the moth Heliothis virescens indicated that
concentration dependency differed between glomeruli
(Galizia et al.,
2000). Our study extends these data by using a larger range of
concentrations. Furthermore, by correlating calcium responses to individual
glomeruli we were able to study qualitative pattern changes in detail.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Animals
Male and female cotton leaf worm moths (S. littoralis, 1–5
days post-emergence) were used in the study. The animals have been reared for
several generations on a potato-based diet
(Hinks and Byers, 1976). The
culture has been supplemented with wild-collected insects yearly for the last
7 years. The pupae were separated according to sex and kept in plastic boxes
at 70% relative humidity, 23°C and a 16 h/8 h light/dark cycle. Adult
moths were supplied with water ad libitum until the start of the
experiment.
Preparation of animals and optical recordings
Preparation of animals and optical recordings were performed as described
elsewhere (Carlsson et al.,
2002). Briefly, a calcium-sensitive dye (CaGR-2-AM; Molecular
Probes, Eugene, OR) was bath applied to the uncovered brain. After incubation
and washing, recordings were carried out in vivo.
We used a TILL Photonics imaging system (Gräfelfing, Germany). Filter settings were dichroic: 500 nm; emission LP 515 nm and the preparation was illuminated at 475 nm. Sequences of 40 frames (4 Hz, 200 ms exposure) were recorded through a 20x (NA 0.50; Olympus, Hamburg, Germany) air objective. Stimulation started at frame 12 and lasted 1 s. Images were binned 2x on chip (to 320 x 240 pixels) to increase signal-to-noise ratio. Execution of protocols and initial analyses of data were made using the software Till-vision (TILL Photonics).
A moistened and charcoal-filtered continuous air stream (30 ml/s)
ventilated the antenna ipsilateral to the recorded AL through a glass tube (7
mm internal diameter). The glass tube ended 
10 mm from the antenna. An
empty Pasteur pipette was inserted through a small hole in the glass tube,
blowing an air stream of 15 ml/s. Air was blown (15 ml/s) through
the odour-laden pipette by a manually triggered puffer device (Syntech,
Hilversum, The Netherlands) for 1 s into the continuous stream of air. During
stimulation the air stream was switched from the empty pipette to the odour
laden one, thereby minimizing mechanical influences. Odorants used in the
experiment were 1-octanol, geraniol, (±)-linalool and
phenylacetaldehyde (PAA). These odorants are biologically relevant to the
animal as common components of green leaves and flowers. The purity of the
compounds was between 95 and 99%. Odorants were dissolved in paraffin oil and
diluted in decadic steps (100 µg/µl–10 ng/µl). Ten microlitres
of diluted odorants were applied on filter papers (5 x 15 mm) in doses
from 100 ng to 1 mg. The filter papers were inserted in Pasteur pipettes, that
were then sealed with Parafilm (American National Can, Chicago, IL) and stored
in a freezer until start of experiment. Control stimuli consisted of filter
paper with solvent only. Every fifth stimulation was made with a control.
Data evaluation
Square regions of interest (10 x 10 pixels) were drawn within the
centre of each glomerulus seen in the anatomical post-stainings (see below).
The size of the square (10 x 10 µm) was well within the
boundaries of glomeruli (50–70 µm diameter), thus minimizing
fluorescence overspill from neighbouring glomeruli. Background fluorescence
(F) was defined as an average of frames 2–11, i.e. before onset
of stimulation. F was subtracted from all frames to yield a
dF and signals were expressed as a relative change in fluorescence
(dF/F) in the regions of interest. A sequence with control
(filter paper with solvent) stimulation was first expressed as relative change
in fluorescence (dF/F) and then subtracted from a sequence
with odour stimulation in order to correct for bleaching and possible solvent
effects. We defined the activity of a glomerulus as the average pixel value of
the mean net activity (dF/F odour stimulation –
dF/F solvent control) during frames 16–22 (peak of
activity).
For correlation analysis we defined a response to an odorant as a multidimensional space where the net activity in each observed glomerulus represents one dimension. The responses were normalized so that the most strongly activated glomerulus for each stimulation was given the value 1. The response profiles for each odorant and concentration were then compared to each other using the Spearman rank correlation test (JMP 4.02; SAS, Cary, NC). A perfect match between stimuli would yield a value of 1 and perfectly complementary responses would yield a value of –1.
Anatomical staining
In order to visualize the glomeruli, which were not visible in the
Ca2+-recordings, we stained the animals with a membrane-bound dye
subsequent to the recordings (Figure
1). We used the voltage-sensitive dye RH 795 (Molecular Probes),
which has previously been used to stain honeybee glomeruli
(Galizia et al.,
1999). Outlines were drawn at the glomerular borders and
transferred to the sequences of raw data in order to make calculations of
activity from individual glomeruli. Certain landmarks, such as remains of
tracheae or the borders of the AL, were used to facilitate the alignment of
the anatomical images with the physiological images.
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Results |
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In eight females, in which all odorants were tested at all concentrations, we managed to anatomically stain the AL after the recordings. Outlines of visible glomeruli were superimposed and aligned with the false-colour-coded images of odour-evoked responses (Figure 1). Certain landmarks, such as tracheae, were visible both in the calcium recordings and in the post-stainings, which facilitated alignment. The number of visible glomeruli we could observe was between 12 and 20 (mean ± SD = 16 ± 3). In all analyses we first superimposed the glomerular outlines on the sequences of optically recorded calcium activity and all subsequent measurements were made within the boundaries of glomeruli.
Focus of activity
A primary question was whether the focus of activity or the principal
glomerulus—i.e. the single glomerulus showing the strongest odour-evoked
[Ca2+] increase—persisted across concentrations.
Figure 1 shows the response
patterns in a single animal to (±)-linalool, geraniol, octanol and PAA
at five concentrations (100 ng–1 mg, in decadic steps) expressed as the
relative change in fluorescence (dF/F). Each image is
false-colour coded, scaled to the upper 50% of its intensity range and
superimposed on grey-scale images from the respective measurement. The
threshold, set to 
50% of the maximal response, excludes low-intensity
activity and noise, but emphasizes the location of the principal glomeruli.
The three alcohols activated overlapping subsets of glomeruli in the lateral
region of the lobe, whereas PAA activated glomeruli in the medial region.
Octanol and geraniol did not elicit any detectable response at the lowest
concentration (100 ng). The single most activated glomerulus was often
different at different concentrations (e.g. PAA and geraniol;
Figure 1). Activity foci were
only persistent across concentrations in 25% of the recorded concentration
series (8 of 32, four odours and eight animals;
Table 1). However, movement of
activity focus was generally restricted to adjacent or proximal glomeruli. The
movement of the principal glomeruli for each of the compounds geraniol,
linalool and octanol occurred to neighbouring glomeruli, also highly activated
by the other alcohols. These glomeruli were all located in the lateral region
of the AL. The principal glomerulus for PAA moved exclusively to neighbouring
glomeruli in the medial region of the AL.
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Dynamic range
In Figure 2, we show an
example of dose–response curves for all glomeruli in a single animal
(same as in Figure 1). In
addition, we identified four glomeruli by their position and response at 100
µg (Carlsson et al.,
2002). The linalool-, geraniol- and octanol-type glomeruli were in
all individuals located in a ventro-dorsal row in the lateral part of the
lobe, with the linalool type located most ventrally and the octanol type most
dorsally. The PAA-type glomerulus was located in the medial part of the AL.
These glomeruli correspond with glomeruli 1, 8, 4 and 16 in
Figure 2, respectively. For the
identified glomeruli, we calculated the mean normalized responses across
animals and concentrations (Figure
3). The most strongly excited glomeruli responded with increasing
intensity over 3–4 log units of concentration. Often, the responses to
the key compounds reached a plateau, suggesting a sigmoid function. Other
glomeruli showed a higher threshold and never reached saturation with the
stimulus doses used in our experiment. Activity in a few glomeruli increased
abruptly, whereafter activity remained at a moderate level with increasing
concentration (e.g. glomerulus 15; Figure
2).
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Number of activated glomeruli
We counted the number of activated glomeruli and expressed them as the
percentage of all visible glomeruli (as observed in subsequent anatomical
stainings). A response in a glomerulus was defined as activity exceeding a
threshold, set to twice the mean standard deviation of prestimulus activity.
The mean percentages of activated glomeruli at five different concentrations
are shown in Figure 4. We found
that the number of activated glomeruli significantly increased with the
concentration [one-way analysis of variance (ANOVA) followed by
Tukey–Kramer HSD]. Percentage data were transformed prior to analysis
using the arcsine method (Sokal and Rohlf,
2000). At the lowest dose, activity was observed in <40% of all
visible glomeruli. The highest dose used in the experiment resulted in
activity in 70–90% of the glomeruli.
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Correlation of responses
First, the net change of fluorescence was calculated for all glomeruli. The activity in each glomerulus represented one dimension in a multidimensional space that constituted the response to a stimulus. The responses were normalized (the strongest activated glomerulus for each stimulation was given a value of 1) and compared to all others using a Spearman rank test (JMP, SAS). A linear correlation test (Pearson) provided similar results.
Correlation indices for all pairs of odours and concentrations were calculated and averaged across animals. The values were colour coded and put into a matrix (Figure 5). Similarity was highest between responses evoked by the same compound. The correlation, however, decreased when the difference in concentration between the stimuli increased. The weakest correlations were found between responses to PAA and the alcohols. In a few instances, the glomerular patterns were actually more similar across odorants than across concentrations. For example, the mean correlation index between responses to 1 mg of geraniol and 1 mg of linalool is significantly higher than the index between responses to 1 mg and 1 µg of linalool (0.78 versus 0.42, P < 0.001; paired t-test, two-tailed distribution; n = 8).Finally, we compared the correlation indices between pairs of odorants at a low (1 µg) and a high (1 mg) dose. A significant increase in correlation at the high concentration for the pairs geraniol–linalool (P < 0.001), geraniol–octanol P < 0.01) and octanol–linalool (P < 0.05) was found (Figure 6; paired t-test, two tailed distribution; n = 8). Thus, patterns evoked by these compounds tend to be more similar to each other at high concentrations. In contrast, comparison with patterns evoked by PAA did not render an increased similarity at high concentrations.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Odour-evoked calcium signals in S. littoralis show a dynamic range of 3–4 log units for the most strongly responding glomeruli. Whereas other studies have reported a concentration-dependent expansion of the focal area of activity due to a recruitment of glomeruli (Rubin and Katz, 1999
;
Johnson and Leon, 2000;
Fuss and Korsching, 2001;
Meister and Bonhoeffer, 2001;
Wachowiak and Cohen, 2001;
Fried et al., 2002),
we show that intensity does not simply increase evenly in all glomeruli.
Instead, the focus of activity often moves between glomeruli across
concentrations. Relative response patterns vary with concentration and get
become identical as the difference in concentration increases. Finally,
correlation of response patterns evoked by different compounds increases with
concentration.
In an earlier study (Carlsson et
al., 2002), we could not prove that the observed localized
foci of odour-evoked activity originated in single glomeruli. Adopting the
post-staining protocol elaborated for honeybees
(Galizia et al.,
1999) to S. littoralis, we can here demonstrate that
activity is indeed confined within boundaries of glomeruli.
Dynamic range
The dynamic range of activity in the glomeruli spanned 3–4 log units.
A similar range is seen in vertebrate imaging studies
(Fuss and Korsching, 2001;
Wachowiak et al.,
2002). Extracellular recordings from single ORNs in S.
littoralis have also revealed dose–response dynamics within the
same range (Ljungberg et al.,
1993; Anderson et al.,
1995). In contrast, receptor neurons in vertebrates generally show
a much narrower range (Duchamp-Viret et al.,
1999,
2000). The expansion of the
dynamic range from single ORNs in the periphery to populations of neurons in
the vertebrate olfactory bulb could be explained if different receptor neurons
detecting the same molecules have different threshold and saturation levels
and converge on the same glomerulus. This is apparently not the case in
insects. The very large family of receptor-coding genes in vertebrates could
possibly contain receptors with similar qualitative tuning, but differing
dynamic ranges.
Dose–response curves often reached a plateau in the most strongly
responding glomeruli, suggesting a sigmoid function. This means that
glomerular responses (and likely ORNs) saturate at high concentrations.
Sigmoid dose–response functions are often observed in single antennal
neurons (Ljungberg et al.,
1993; Anderson et al.,
1995). Some glomeruli, however, showed moderate activity at low
concentrations, but no further increase at higher doses (see below).
Activity focus
We showed in an earlier study (Carlsson
et al., 2002) that even if odour-evoked activity was
distributed in a large number of glomeruli, each odorant preferentially
activated a single glomerulus (or a few glomeruli). A single concentration
was, however, used for all compounds tested. Here, we show that the principal
glomeruli are often not consistent across concentrations, but rather move to
neighbouring glomeruli. A focal movement is the result of different
concentration-dependency among glomeruli. Saturation is reached at different
concentrations and the slopes of the dose–response curves differ. A
possible explanation of why a focal shift of activity generally resulted in a
neighbouring glomerulus becoming the most activated is that ORNs expressing
receptor molecules with overlapping receptive ranges project to adjacent
glomeruli. In fact, axons of vertebrate ORNs expressing homologous and closely
linked receptor genes arborize in neighbouring glomeruli
(Tsuboi et al.,
1999). Concentration-dependent movement of principal glomeruli has
also been observed in mice (Fried et
al., 2002). In the latter study, ORNs were selectively
stained with a calcium-sensitive dye. This means that the focal shift in the
mouse was exclusively attributed to activity in the ORN terminals. In
honeybees, on the other hand, the same principal glomeruli persisted across
concentrations (Sachse et al.,
1999). However, we used a wider range of concentrations and far
lower doses and the results can thus not be directly compared.
Glomerular recruitment
With higher stimulus concentration, an increasing number of glomeruli were
activated. It is remarkable that even at the lowest concentration, linalool,
for example, excited 40% of all visible glomeruli and at the highest
concentration virtually all. This could, to some extent, be due to responses
in multiglomerular local interneurons (LNs) or responses in projection neurons
(PNs) arborizing in glomeruli not innervated by responding ORNs. Even though a
bath application of the calcium-sensitive dye is non-selective with respect to
the type of neuron, afferent-selective staining methods have also revealed
responses in a very large population of glomeruli
(Friedrich and Korsching,
1997; Fuss and Korsching,
2001; Wachowiak and Cohen,
2001; Fried et al.,
2002) The increase in the number of responding glomeruli with
concentration likely reflects a recruitment of ORN types detecting a specific
compound. These ORNs have a low affinity and are only activated at high
concentrations. Plant-odour-responding ORNs in S. littoralis respond
to a broader spectrum of compounds at higher concentrations
(Anderson et al.,
1995). Even pheromone-specific neurons can respond to
non-pheromones if the concentration is high enough
(Hansson et al.,
1989; Carlsson and Hansson,
2002). A recruitment of responding glomeruli with increasing
concentration has also been observed in optical imaging studies in vertebrates
(Rubin and Katz, 1999;
Johnson and Leon, 2000;
Fuss and Korsching, 2001;
Meister and Bonhoeffer, 2001;
Wachowiak and Cohen, 2001;
Fried et al., 2002)
and, recently, in fruitflies (Wang et
al., 2003).
Correlation of glomerular patterns
When odour-evoked activity patterns for different concentrations of the
same compound were normalized (i.e. not considering absolute intensity), it
became clear that the relative patterns were not identical. Instead, we found
a decrease in pattern similarity when the difference in concentration between
the stimuli increased. Furthermore, as has been reported in vertebrates
(Fuss and Korsching, 2001), we
found that activity patterns evoked by different compounds become more similar
at high concentrations. However, this effect seems to depend on the similarity
of the odorants, i.e. if they overlap in molecular structure. Geraniol,
linalool and octanol all have an attached alcohol group as a common
denominator and do not have a cyclic structure, whereas PAA consists of a
benzene ring with an attached aldehyde group.
Recently, it was found (Ng et
al. 2002), using a binary glomerular coding scheme, that the
distance between responses to different compounds actually increased with
concentration in Drosophila. The stimuli used were fruit odours that
are complex mixtures of volatiles. Thus, differing analysis methods and choice
of stimuli make it difficult directly to compare the results.
Several different factors may contribute to the concentration-dependent
pattern changes. First of all there is a recruitment of glomeruli at increased
concentration (as discussed above). Secondly, activity in insect ORNs
saturates at high stimulus concentrations due to adaptation
(Todd and Baker, 1999). If an
ORN is saturated by its key compound, other neurons may respond equally
strongly and the original across-neuron ratio changes. Furthermore, when an
ORN is saturated at high doses by its key compound, a second-best stimulus may
excite the neuron equally well. Geraniol, linalool and octanol activate
overlapping subsets of ORNs in S. littoralis
(Anderson et al.,
1995). This means that the ratio between the active neurons may
change at high concentrations and the odour-unique, across-neuron pattern may
become less distinctive for these compounds. The levelling
concentration–response functions
(Figure 2) show that activity
in certain glomeruli saturates at high concentrations. Thirdly, in some
glomeruli saturation was already reached at intermediate doses. One reason for
this may be that responding ORNs do not directly innervate these glomeruli.
Instead, the signals observed might come from LNs, connecting glomeruli
innervated by responding ORNs and those that are not. LNs connect either most
or all glomeruli in the lobe with equally dense innervation, or connect only a
few glomeruli with innervation biased to a single glomerulus
(Anton and Homberg, 1999). Even
though calcium imaging, using a bath application of the dye, emphasizes ORN
activity (Galizia et al.,
1998), part of the measured signal likely derives from AL
interneurons. In contrast to ORNs, LNs and PNs are often much less
concentration-dependent and many interneurons do not express increased spike
activity at concentrations above threshold levels
(Anton et al., 1997;
Masante-Roca et al.,
2002). An alternative explanation for saturation at intermediate
concentrations is that responding ORNs innervate these glomeruli, but are
presynaptically inhibited, a mechanism demonstrated in crustaceans (Wachowiak
and Cohen, 1998,
1999).
Olfactory coding and perception
Concentration changes affect not only the intensity of signals in the
glomeruli, but also the spatial distribution of activity. Odour-evoked
representations in different combinations of glomeruli have been suggested to
be a code for odour identity (Johnson
et al., 1998; Galizia
et al., 1999), which would then be decoded in higher
brain centra by computing the ratio of activity among the glomeruli. If such a
ratio varies due to fluctuations in concentration, then the decoding of the
odour identity may be complicated. Assuming that a combinatorial glomerular
code underlies the qualitative perception of an odour, confusion may occur
when trying to identify an odour at different concentrations. Perceived odour
quality in humans has been shown to vary with concentration
(Gross-Isserof and Lancet,
1988; Arctander,
1994). However, it is not a common phenomenon as most odours are
described as qualitatively invariant regardless of concentration. Honeybees
can easily be trained to respond to odours and by using a differential
training paradigm, with one odour coupled with a reward and the other not,
discriminatory ability can be studied. Bhagavan and Smith
(Bhagavan and Smith, 1997)
showed that bees trained to a high concentration of an odorant had a lower
tendency to generalize between the trained and a novel odour than bees trained
to a low concentration. This indicates that the discriminatory ability
actually increases at high concentrations. Even though this seemingly
contradicts our results, precise information about the odour quality may still
be present in the population of PNs. On the other hand, it cannot be ruled out
that the spatial patterns of glomerular activity play a less important role in
odour encoding than the temporal characteristics of the signals. If this is
so, odour quality could be correctly coded in the temporal patterns at
different concentrations, no matter if the spatial patterns vary. Recently,
Spors and Grinvald (Spors and Grinvald,
2002) demonstrated in rats, using a fast voltage-sensitive dye,
that even though glomerular recruitment occurred, the added glomeruli had
longer latencies and the initial pattern and the sequence of glomerular
activation were conserved across concentrations. Thus, Spors and Grinvald
suggested that qualitative information is contained in the sequencing of
activity, whereas information about concentration is carried by the latencies.
Analysis of dynamic aspects of the glomerular patterns was, however, limited
by the temporal resolution in our experiment.
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Acknowledgments |
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We would like to thank Drs Peter Anderson, Sylvia Anton and Jocelijn Meijerink for discussions and critical review of the manuscript. The research was supported by EU FET-IST programme Project No. IST-2001-33066 and the Swedish Research Council.
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Accepted March 5, 2003
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