Chem. Senses 28: 279-284,
2003
© Oxford University Press 2003
Extreme Sensitivity in an Olfactory System
Department of Experimental Biology, Section of General Physiology, University of Cagliari, Monserrato–Cagliari, Italy 1 Department of Crop Science, Division of Chemical Ecology, Swedish University of Agricultural Sciences, Alnarp, Sweden
Correspondence to be sent to: Anna Maria Angioy, Department of Experimental Biology, Section of General Physiology, University of Cagliari, Monserrato–Cagliari, Italy. e-mail: amheart{at}unica.it
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
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We recorded olfactory-induced cardiac responses to evaluate olfactory response thresholds to behaviourally relevant odours in a moth. Specific antennal receptor neurons enable insects to detect biologically meaningful odours such as sex pheromones and host-plant volatiles. The response threshold values demonstrated here are well below anything earlier reported in any organism. A heart response was triggered by less than six molecules of the most efficient odours hitting the antennae of the insect. The behavioural significance of this extreme sensitivity most likely lies in the creation of awareness and readiness to respond behaviourally at higher concentration levels.
Key words: moth, sex pheromone, plant odours, cardiac response
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The olfactory system has become an important model system regarding sensory detection and integration. In this context, insects represent an important source of information regarding fundamental principles of olfactory detection (Ziegelberger, 1995
;
Clyne et al., 1999;
de Bruyne et al.,
1999,
2001;
Vosshall et al.,
1999; Störtkuhl and
Kettler, 2001) and central nervous information processing (Hansson
et al., 1991,
1992;
Stopfer et al., 1997;
Ito et al., 1998;
Christensen et al.,
2000; Dubnau et al.,
2001; McGuire et al.,
2001). Extensive investigations of the anatomy and function of the
olfactory system of moths have provided a very useful model for
neuroethological studies (Hartlieb and
Anderson, 1999). Moth olfactory receptor neurons (ORN) exhibit a
high degree of selectivity and sensitivity to both pheromone and non-pheromone
volatiles, thus supplying the brain with high-quality information on odour
identity, intensity and spatiotemporal distribution
(Hansson et al.,
1992; Hansson,
1995; Christensen et al.,
1996,
2000;
Hansson and Christensen, 1999;
Vickers et al.,
2001). For instance, the high sensitivity to the female-produced
sex pheromone exhibited by the silk moth (Bombyx mori) male allows it
to respond behaviourally when just 85 ORNs/antenna intercept one molecule each
per second (Kaissling and Priesner,
1970; Kaissling,
1971). On the other hand, much higher stimulus intensities are
generally reported as minimum values needed for recording significant activity
from ORNs (Kaissling, 1987),
CNS neurons (Hansson and Christensen,
1999), as well as for driving an appropriate insect behaviour
(Todd and Baker, 1999).
Odour detection induces cardiac responses that have been described as a
sensitive tool for testing insect olfactory reactivity
(Queinnec and Campan, 1976).
Analogous responses also occur following stimulation of types of sensory
receptors, such as visual (Thon,
1982), gustatory (Angioy,
1988) and mechanical (Ai and
Kuwasawa, 1995). On the basis of facilitatory influence on motor
activity, heart responses to visual stimulation were suggested to play a
preparatory role for ensuing behaviour
(Thon, 1982). Short cardiac
response latencies (<1 s) suggest that sensory input activates a reflex
control mechanism (Thon, 1982;
Angioy, 1988;
Angioy et al., 1987)
along cardiac innervation (Davis et
al., 2001). In blowflies, an immediate arrest of a fast phase
activity and a prompt setting in of a slower one occur after olfactory
stimulation with several kinds of volatiles
(Angioy et al., 1987).
In Heliothis virescens moths, a sudden shift from a low-frequency
phase of cardiac activity to a high-frequency one follows stimulation with
sex-pheromone or 1-hexanol molecules at concentrations below threshold values
eliciting behavioural responses (Angioy
et al., 1998).
Here we show an extremely high sensitivity of cardiac responsiveness to sex pheromone and plant odour information in both sexes of the cotton leaf worm moth, Spodoptera littoralis, an olfactory sensitivity higher than ever reported before. S. littoralis is a noctuid moth that has been very well investigated concerning olfactory function and olfactory induced behaviour. Specific receptor neurons tuned to the odours used in the present study have been identified on the antenna. Unlike most other moths, the female also possess a well-developed sense for the sex pheromone components produced by herself. The function of this autodetection is so far unknown.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Insects
Experiments were performed on 2–5-day-old adults of S.
littoralis. Larvae were obtained from the Swedish University of
Agricultural Sciences in Alnarp, Sweden and reared on a semi-synthetic diet
(Hinks and Byers, 1976) using
potatoes instead of beans. Moths were separated by sex at the pupal stage, put
into emergence boxes and kept in a cabinet at 24°C, 70–80% relative
humidity, 7/17 night/day cycle. Adults were kept without food, but were
provided with water ad libitum during the 24 h prior to
experiments.
Moths were fixed dorsal side up on a strip of low melting point dental wax; both wings and legs were immobilized. Using soft wet paper, cuticular scales were removed from small areas of the mesothoracic and abdominal dorsal body surfaces to allow positioning of the electrodes. Each moth was placed on a microscope stage in the visual field of a stereomicroscope (Wild M5A; Wild Leitz Ltd, Heerbrugg, Switzerland) within a Faraday shield on an antivibration surface.
Cardiac activity recording
Monopolar extracellular electrocardiograms (ECGs) were performed on intact specimens using a pair of metal electrodes (Ag–AgCl wires, 250 µm diameter) in contact with the insect cuticle by means of a conductive ECG gel. The active electrode, connected to an amplifier (Altech Electronics, Italy), was positioned on the fourth abdominal segment. The ground electrode was placed on the mesothorax. Signals were displayed on the screen of an oscilloscope (Tektronix 5111A; Tektronix Inc. Beaverton, OR), stored on a modified video recorder (Vetter; A.R. Vetter Co. Inc. Rebesburg, PA) and later analysed with an integrated system of hardware and software (MacLab System; AD Instruments Ltd, Castle Hill, Australia).
Olfactory stimulation
A main flow of humidified and charcoal-filtered air (1.70 l/min) was
continuously delivered through a glass tube (i.d. 8 mm), ending 2 cm in front
of the moth antennae. The tip of a Pasteur pipette, containing a 7 x 15
mm piece of filter paper with (stimulus) or without (control) an olfactory
stimulus, was inserted into a small opening in the glass tube, 70 mm from the
antennae. By means of a mechanical puffing device (Altech Electronics, Italy),
a 1 s air pulse (0.50 l/min) was then sent through the Pasteur pipette. A
glass funnel (i.d. 5 cm) connected to an air suction line was positioned close
to the preparation to take away the odour-carrying air after stimulation. The
following odour stimuli were tested: three plant odours, geraniol, indole and
±linalool; female-emitted sex pheromone volatiles—the minor
component [(Z,E)-9,12-tetradecadienyl acetate
(Z9,E12–14:OAc)], the major component
[(Z,E)-9,11-tetradecadienyl acetate
(Z9,E11–14:OAc)] and their blend in the proportion of
1:99, equivalent to that measured in the natural sex pheromone by Kehat and
Dunkelblum (Kehat and Dunkelblum,
1993). Chemicals were diluted in hexane in decadic steps and
tested in order of increasing concentration after solvent evaporation. The
solubilization of indole in hexane was obtained by stirring and slightly
heating the solution in sealed vials. Plant odours and pheromone compounds
were tested on separate groups of specimens, each group comprising a minimum
of 10 moths of each sex.
Experimental procedure
Cardiac activity was monitored after a 15 min period of recovery from
electrode positioning. If heart activity was still affected by spontaneous
movements of the insect (Thon,
1982), additional recovery time was allowed until regular cardiac
activity was observed. Continuous ECG recording started three cardiac cycles
before delivery of the main air flow. This air flow permanently flushed the
antennae until the end of tests on each moth. Control and blank stimulations
were performed both at the beginning and at the end of the experimental
session by using empty pipettes and solvent-loaded pipettes after solvent
evaporation, respectively. Animals displaying a response to background stimuli
were removed from the experimental group. A single olfactory stimulation was
delivered during a cardiac cycle, at the beginning of a fast or slow phase.
For each experimental group, a given chemical was tested in increasing order
of concentration until a cardiac response was measured. Subsequent
stimulations were separated by a 3 min pause to avoid receptor adaptation
(Kaissling, 1987). Sequences
of stimulation with different odours were separated by 15 min intervals to
limit possible habituation phenomena
(Thon, 1982).
Data analysis
Regular cardiac activity of male (n = 11) and female (n = 19) moths in the absence of stimulation was evaluated by measuring cardiac phase duration and signal frequency at the beginning, at the end and at each quarter of phase duration. Values are expressed as means ± SE. Levels of significance of sex-related differences were determined by an unpaired Student's t-test between groups. For each experimental group and odour tested, the cardiac response threshold was set to the amount of odour applied on a filter paper to which >50% of the specimens tested showed a cardiac response. Latency of the cardiac response was measured as the time interval between the initiation of the stimulus and the occurrence of variations in activity, as shown in the electrocardiogram.
Approximate numbers of molecules added to the stimulus filter paper were calculated by multiplying the amount added in grams with Avogadro's number (1 mol = 6 x 1023 molecules) and dividing the number arrived at by the mol. wt of the substance added.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In absence of stimulation, electrocardiograph activity of S. littoralis took the form of a cyclic alternation between high- and low-frequency phasic bursts (Figure 1A). These phases were termed the fast phase and the slow phase, respectively (Angioy et al., 1998
). Analysis of signal patterns recorded in 19 females and 11
males showed that the heartbeat pattern did not differ between the sexes,
except that females generally exhibited a higher frequency of cardiac signals
(Figure 1B). An isoelectric
period lasting several seconds was recorded at the end of the fast phase in a
limited number of males (three) and females (four).
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On initiating the main and continuous flow of pure air across the animal's
antennae at the beginning of a slow phase, an immediate increase in the
frequency of cardiac signals was observed (S1 in
Figure 2A). The slow phase
reverted to a characteristic fast phase. Therefore, in Spodoptera, as
well as in other insect species (Angioy
et al., 1998), tachycardia results from antennal
mechanosensory stimulation caused by the arrival of pure air. This effect was
transitory and a regular slow phase subsequently set in even when the main air
flow continued to reach the moth's antennae, a result most probably due to
mechanoreceptor adaptation. Addition of a secondary air flow did not modify
the subsequent slow phase (S2 in
Figure 2A). In all insects
tested (>100) mechanoreceptor stimulation with the air flow was followed by
a tachycardia response only when stimulation was carried out during a slow
phase. Stimulation during a fast phase had no effect (S1 in
Figure 2B).
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As following primary mechanosensory stimulation, reversion of slow-phase
activity resulted from olfactory stimulation with the tested sex pheromone- or
plant-related chemicals (Figures
3A and
4A). The latency time from
stimulation to response was 
1 s. No alteration in activity followed
olfactory stimulation applied during a fast phase. The dose–response
curves obtained after stimulating moths with increasing amounts of the major
or minor component of the sex pheromone, or a behaviourally relevant blend of
these, reveal extremely low response thresholds, but also sex-related
differences in cardiac responsiveness
(Figure 3B). In >50% of the
male moths tested, the cardiac response occurred at doses of
10–19 g of the blend and of the major component
(Z9,E11–14:OAc), and of 10–17 g of
the minor component (Z9,E12–14:OAc). In female moths,
doses of equivalent effectiveness were 10–17 g of the blend,
10–14 g of the major component and 10–9 g of
the minor component. In the female, threshold levels were thus 102,
105 and 108 times higher than in the male for the major
component, minor component and blend stimulus, respectively.
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As regards the plant odours tested, doses amounting to 10–18 g of geraniol and 10–16 g of indole evoked cardiac response in >50% of moths of both sexes (Figure 4B). Doses of ±linalool amounting to 10–12 and 10–7 g were necessary to induce a cardiac response in 50% of males and females, respectively. Only for ±linalool was a sex-related difference observed, where the male responded at 105 times lower concentration than did the female.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Monitoring of olfactory-induced cardiac responses in order to evaluate detection levels of odours turned out to be an effective experimental strategy. The response of the Spodoptera heart accurately indicates odour perception, even when volatiles are delivered in amounts substantially below those required for obtaining an observable behavioural response (Anderson et al., 1993
). Extremely low amounts of sex pheromone compounds were
sufficient to induce responses in a significant number of males.
10–19 g, i.e. 240 molecules, of the pheromone blend
applied to the stimulus filter paper were sufficient to elicit a response in
>50% of the males. At an absolute maximum, 10% of the molecules, i.e.
24 molecules, will leave the filter paper during the stimulus period. The
antennae cover 25% of the outlet of the stimulus tube, bringing the
number of molecules potentially hitting an olfactory sensillum on the antenna
down to about six. The detection level is thus of a magnitude well below what
has earlier been calculated as being necessary to induce a behavioural
response in the silk moth (Kaissling and
Priesner, 1970) and at a magnitude almost impossible to imagine.
We therefore repeated our series of experiments three times on separate groups
of 10 insects each, but arrived at the same result each time. The difference
between response thresholds recorded in Bombyx and
Spodoptera may depend on a higher sensitivity of the cardiac response
method compared to measuring behavioural responses through wing vibration
observations. Differences might also reside in the stimulating systems
adopted. Interestingly, a highly sensitive female response to its own
pheromone was also demonstrated, a phenomenon consistent with the fact that
females possess ORNs (Ljungberg et
al., 1993; Anderson et
al., 1995; Jönsson
and Anderson, 1999) and antennal lobe neurons
(Anton and Hansson, 1995)
selectively sensitive to sex-pheromone stimulation. This observation
highlights the need for future behavioural investigations, as the significance
of the autodetection of pheromone so far is unknown. However, a higher
response threshold to pheromone was found in the female. The sensitivity of
sex-pheromone-specific ORNs is equivalent in the two sexes, the receptor
threshold being in the range 10–8–10–7
g of stimulus loaded onto filter paper, while the number of pheromone sensilla
is lower in the female (Ljungberg et
al., 1993). The male pheromone-detecting system thus displays
a higher rate of convergence of ORNs onto AL neurons, which can explain the
lower male response threshold in heart recordings. The finding that the female
response threshold to the pheromone blend is much lower than to single
components indicates the synergistic effect of the two components. On the
other hand, the male response thresholds to the blend and to the major
pheromone component were equivalent, even though the presence of the complete
blend is known to be imperative for attraction to occur. In spite of these
sex-related differences in information processing, males and females shared
the characteristic of having a cardiac response threshold much lower than that
of ORNs. This finding highlights the strong convergence and sensitivity
amplification that takes place within the moth olfactory system.
The recordings also showed that plant-associated odours were detected at
very low concentrations, suggesting that the pheromone-detecting system is not
unique in its sensitivity. The detection threshold for geraniol was <390
molecules applied to the stimulus filter paper and, consequently, <10
molecules hitting the antenna. S. littoralis moths have specific ORNs
tuned to each of the three compounds tested (Anderson et al.,
1993,
1995;
Jönsson and Anderson,
1999) and some antennal lobe neurons respond with high specificity
to them (Anton and Hansson,
1995). The response threshold of antennal ORNs specific to
plant-produced odours is in the same range as in ORNs tuned to pheromone
components. In S. littoralis females, it is
10–9 g (Jönsson
and Anderson, 1999). The lower sensitivity to linalool correlates
well with the fact that ORNs tuned to this compound are significantly less
sensitive compared to those tuned to geraniol
(Anderson et al.,
1993) and indole (Jönsson
and Anderson, 1999). Receptor neurons detecting linalool are
present in higher numbers in male antennae, while being quite rare in the
female. The consequent difference in sensory input after linalool stimulation
may thus account for the lower cardiac reactivity detected in females.
Our experimental results show that moths display an olfactory sensitivity
even more pronounced than that suggested from theoretical calculations. In the
male pheromone-detecting system around five molecules and in the
plant-odour-detecting system 10 molecules potentially hitting the antenna
during 1 s are enough to trigger a heartbeat frequency change. This result
demonstrates that the moth olfactory system has evolved a sensitivity beyond
any other chemosensory detection systems known today. No direct behavioural
response has been registered at the low concentrations applied in the present
study. The significance of the heart rate change can most likely be found in
the formation of awareness regarding the presence of a certain stimulus and a
readiness to respond behaviourally.
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Acknowledgments |
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We thank Elisabeth Marling, SLU, for rearing insects. Supported by a Socrates-EU Grant, the Italian Ministry of University and Scientific Research and the Swedish Science Research Council.
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References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Ai, H. and Kuwasawa, K. (1995) Neural pathways for cardiac reflexes triggered by mechanical stimuli in larvae of Bombyx mori. J. Insect Physiol.,41 ,1119 –1131.[CrossRef]
Anderson, P., Hilker, M., Hansson, B.S., Bombosch, S., Klein, B. and Schildknecht, H. (1993) Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): a behavioural and electrophysiological evaluation. J. Insect Physiol., 39,129 –137.[CrossRef]
Anderson, P., Hansson, B.S. and Löfqvist, J. (1995) Plant-odour-specific receptor neurones on the antennae of female and male Spodoptera littoralis. Physiol. Entomol., 20,189 –198.
Angioy, A.M. (1988) Reflex cardiac response to a feeding stimulus in the blowfly Calliphora vomitoria L.J. Insect Physiol. , 34,21 –27.[CrossRef]
Angioy, A.M., Tomassini Barbarossa, I., Crnjar, R., Liscia, A. and Pietra, P. (1987) Reflex cardiac response to various olfactory stimuli in the blowfly, Protophormia terraenovae.Neurosci. Lett. , 81,263 –266.[CrossRef][Web of Science][Medline]
Angioy, A.M., Tomassini Barbarossa, I., Orrù, S. and Kaissling, K.-E. (1998) Cardiac responses to sensory stimulation in the adult tobacco budworm moth, Heliothis virescens.J. Comp. Physiol. A , 182,299 –305.[CrossRef]
Anton, S. and Hansson, B.S. (1995) Sex pheromone and plant-associated odour processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae). J. Comp. Physiol. A,176 ,773 –789.
Christensen, T.A., Heinbockel, T. and Hildebrand, J.G. (1996) Olfactory information processing in the brain: encoding chemical and temporal features of odors. J. Neurobiol., 30,82 –91.[CrossRef][Web of Science][Medline]
Christensen, T.A., Pawlowski, V.M., Lei, H. and Hildebrand, J.G. (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nature Neurosci., 3,927 –931.[CrossRef][Web of Science][Medline]
Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J. and Carlson, J.R. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila.Neuron , 22,327 –338.[CrossRef][Web of Science][Medline]
Davis, N.T., Dulcis, D. and Hildebrand, J.G. (2001) Innervation of the heart and aorta of Manduca sexta. J. Comp. Neurol., 440,245 –260.[CrossRef][Web of Science][Medline]
de Bruyne, M., Clyne, P.J. and Carlson, J.R.
(1999) Odor coding in a model olfactory organ: the
Drosophila maxillary palp. J. Neurosci.,19
,4520
–4532.
de Bruyne, M., Foster, K. and Carlson, J.R. (2001) Odor coding in the Drosophila antenna.Neuron , 30,537 –552.[CrossRef][Web of Science][Medline]
Dubnau, J., Grady, L., Kitamoto, T. and Tully, T. (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory.Nature , 411,476 –480.[CrossRef][Medline]
Hansson, B.S. (1995) Olfaction in Lepidoptera. Experientia, 51,1003 –1027.[CrossRef][Web of Science]
Hansson, B.S. and Christensen T.A. (1999) Functional characteristics of the antennal lobe. In Hansson, B.S. (ed.), Insect Olfaction. Springer, Berlin, pp.125 –161.
Hansson, B.S., Christensen, T.A. and Hildebrand, J.G. (1991) Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J. Comp. Neurol., 312,264 –278.[CrossRef][Web of Science][Medline]
Hansson, B.S., Ljungberg, H., Hallberg, E. and
Löfstedt, C. (1992) Functional specialization of
olfactory glomeruli in a moth. Science,256
,1313
–1315.
Hartlieb, E. and Anderson, P. (1999) Olfactory-released behaviours. In Hansson, B.S. (ed.), Insect Olfaction. Springer, Berlin, pp.315 –349.
Hinks, C.F. and Byers, J.R. (1976) Biosystematics of the genus Euoxa (Lepidoptera: Noctuidae). V. Rearing procedures and life cycles of 36 species. Can. Ent., 108,1345 –1357.
Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D.
and Strausfeld, N.J. (1998) The organization of
extrinsic neurons and their implications in the functional roles of the
mushroom bodies in Drosophila melanogaster Meigen. Learn.
Mem., 5,52
–77.
Jönsson, M. and Anderson, P. (1999) Electrophysiological response to herbivore-induced host plant volatiles in the moth Spodoptera littoralis. Physiol. Entomol.,24 , 377–385.[CrossRef]
Kaissling, K.-E. (1971) Insect olfaction. In Beidler, L.M. (ed.) Handbook of Sensory Physiology, Vol. IV. Springer, Berlin, pp.351 –431.
Kaissling, K.-E. (1987) Stimulus transduction. In Colbow, K. (ed.), R.H. Wright Lectures on Insect Olfaction. Simon Fraser University, Burnaby BC, Canada, pp.17 –32.
Kaissling, K.-E. and Priesner, E. (1970) Die Riechschwelle des Seidenspinners.Naturwissenschaften , 57,23 –28.[CrossRef][Web of Science][Medline]
Kehat, M. and Dunkelblum, E. (1993) Sex pheromones: achievements in monitoring and mating disruption of cotton pests in Israel. Arch. Insect Biochem. Physiol.,22 , 425–431.[CrossRef]
Ljungberg, H., Anderson, P. and Hansson, B.S. (1993) Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae). J. Insect Physiol.,39 , 253–260.[CrossRef]
McGuire, S.E., Le, P.T. and Davis R.L.
(2001) The role of Drosophila mushroom body
signaling in olfactory memory. Science,293
, 1330–1333;
published online 7 June 2001 (10.1126/science.1062622).
Queinnec, Y. and Campan, M. (1976) Influence de la maturité sexuelle sur l'activité et la réactivité cardiaque de Calliphora vomitoria (Diptera, Calliphoridae). II. Analyse des rèponses olfacto-cardiaques.J. Physiol. (Paris) , 72,903 –916.
Stopfer, M., Bhagavan, S. and Laurent, G. (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature,390 , 70–74.[CrossRef][Medline]
Störtkuhl, K.F. and Kettler, R.
(2001) Functional analysis of an olfactory receptor in
Drosophila melanogaster. Proc. Natl Acad. Sci. USA,98
,9381
–9385.
Thon, B. (1982) Influence of the cardiac phase on the latency of a motor response to a visual stimulus in the blowfly. J. Insect Physiol., 28,411 –416.[CrossRef]
Todd, J.L. and Baker, T.C (1999) Function of peripheral olfactory organs. In Hansson, B.S. (ed.),Insect Olfaction . Springer, Berlin, pp.67 –96.
Vickers, N.J., Christensen, T.A., Baker, T.C. and Hildebrand, J.G. (2001) Odour-plume dynamics influence the brain's olfactory code. Nature,410 ,466 –470.[CrossRef][Medline]
Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A. and Axel, R. (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell,96 , 725–736.[CrossRef][Web of Science][Medline]
Ziegelberger, G. (1995) Redox-shift of the pheromone-binding protein in the silkmoth Antheraea polyphemus.Eur. J. Biochem. , 232,706 –711.[Web of Science][Medline]
Accepted March 11, 2003
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