Chem. Senses 26: 1133-1138,
2001
© Oxford University Press 2001
Is Feeding Behaviour in Crucian Carp Mediated by the Lateral Olfactory Tract?
Division of General Physiology, Department of Biology, PO Box 1051, University of Oslo, N-0316 Oslo, Norway 1 Department of Ichthyology, Biological Faculty, Moscow State University, R-119 899, Russia
Corresponding author: Kjell B. Døving, Division of General Physiology, Department of Biology, PO Box 10561, University of Oslo, N-0316 Oslo, Norway. e-mail: kjelld{at}bio.uio.no
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Abstract |
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Experiments were performed to investigate which bundle of the olfactory tract was essential for mediating feeding behaviour in crucian carp. Fish were divided in three groups: control fish, fish with only the lateral olfactory tracts (LOTs) intact and fish with the LOTs cut. The fish were maintained in physiological saline after surgery to preserve the remaining tracts and postoperative inspections revealed the functional status of the remaining tracts. With the injection of food odour into the aquaria the scores for various feeding behaviours—biting, snapping, mouth openings and vertical posture—were not significantly different between those of the control fish and the fish with the LOT intact. Those fish that had the LOT cut but the medial and lateral parts of the medial olfactory tract (mMOT, lMOT) intact had significantly lower feeding-related scores than the other two groups of fish. The results of the present study indicate that the LOT is necessary to maintain the full qualitative and quantitative extent of feeding behaviour in crucian carp.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The olfactory system in fish mediates a number of behaviours that are essential for life processes: feeding, reproduction and alarm. In gadids, silurids and cyprinids, the olfactory tracts are well suited for experimental manipulations as both tracts are long and divided into distinct bundles (Sheldon, 1912
). Each bundle
connects to different areas of the brain and this organization is indicative
of separate functional properties for each bundle, even though there are
anatomical overlaps in projections seen in both carp, Cyprinus carpio
(Ichikawa, 1975;
von Bartheld et al.,
1984; Levine and Dethier,
1985), and cod, Gadus morhua,
(Rooney et al.,
1992).
The functional implication of these projections has already been
demonstrated by experiments involving electrical stimulation of discrete
bundles of the olfactory tract in free swimming cod
(Døving and Selset,
1980). Feeding behaviours were elicited by stimulation of the
lateral olfactory tracts (LOTs), while spawning behaviour was induced by
electrical stimulation of the lateral bundle of the medial olfactory tracts
(lMOTs). Alarm-related behaviour, on the other hand, was seen in cod when
electrical pulses were applied to the medial bundle of the medial olfactory
tracts (mMOTs). Further evidence for the functional separation of olfactory
tracts can be found in behavioural experiments with goldfish, Carassius
auratus, which had been trained to discriminate amino acids and lost this
ability after the transection of their LOTs
(von Rekowski and Zippel,
1993). This functional partitioning has also been demonstrated in
goldfish as courtship behaviour is mediated by the medial olfactory tracts
(MOTs) (Stacey and Kyle, 1983;
Kyle et al., 1987).
Sex pheromones selectively elicited electrical activity in medial olfactory
tracts of male goldfish (Sorensen et
al., 1991), whereas sperm release was induced by electrical
stimulation of the medial olfactory tracts
(Demski and Dulka, 1984). Alarm
reaction in crucian carp Carassius carassius, also exhibit functional
partitioning as this reaction is mediated by the mMOT
(Hamdani et al.,
2000).
These experiments lay the foundation for the hypothesis that each bundle of
the olfactory tract mediates a certain class of behaviour
(Kotrschal, 2000). Some
experiments, however, have provided conflicting evidence, as shown in the
study by Stacey and Kyles on goldfish, which found that either the MOT or the
LOT maintained intact levels of feeding response to food odours (Stacey and
Kyles, 1983). As mentioned, this observation is in conflict with the general
idea of a functional specificity of each olfactory tract bundle, and we
therefore found it important to reinvestigate the functional specificity of
the LOT as a pathway for various feeding behaviours. In the present study we
present evidence that the LOT is necessary to maintain the full qualitative
and quantitative extent of feeding behaviour in crucian carp.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Crucian carp, C. carassius L., were caught in a small lake just outside the Oslo city boundry. They were transported to the aquarium facilities at the Department of Biology. The 12 crucian carp used for these experiments weighed between 15 and 22 g. All rearing and experimental procedures were conducted in accordance with the protocols described by the University of Oslo Animal Care Committee in order to respect the welfare of our experimental animals.
Experimental design
In view of the results from cod experiments indicating that the LOT
mediates feeding behaviour (Døving
and Selset, 1980) and the loss of discriminating behaviour seen by
cutting the LOT in goldfish (von Rekowski
and Zippel, 1993), we decided to study the feeding behaviours
elicited by food odours in three groups of fish: controls, fish with only the
LOT intact and fish with only the LOT cut. Three groups of fish were observed
for a period of 2 min while injecting either physiological saline or food
extract to the aquaria. Observations were made twice a day for 7 days starting
1 week after surgery.
Surgical operation
The fish were anaesthetized with benzocaine (45 mg/l), placed in a stand
with running water through the mouth and over the gills, and operated on under
a stereomicroscope. The skin just above the olfactory tracts was cut open and
a portion of the dorsal cranium removed. The mesenchymeal tissue in the brain
case was aspirated and the meninges around the olfactory tracts were removed
with fine forceps. The olfactory tracts were clearly visible as three distinct
bundles running from the olfactory bulb to the brain
(Figure 1). The bundles were
gently separated, taking care not to disrupt blood vessels. When cutting
particular bundles of the olfactory tracts, care was taken to remove 
2 mm
to prevent regeneration (von Rekowski and
Zippel, 1993; Zippel et
al., 1993). We visually inspected the fibre bundles to
control possible regeneration at the end of the experiments. The bundles of
the olfactory tracts were cut symmetrically on both sides as follows:
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- Two fish were sham operated, i.e. the brain case was opened and the
meninges were removed to see the olfactory tracts, and two fish were
anesthetized only. These four fish served as control.
- In four fish the LOT was left intact while the lMOT and mMOT were
sectioned.
- In four fish the LOT was cut, while both the mMOT and the lMOT were left
intact.
After sectioning the appropriate bundles, the cranial cavity was filled with a 2% solution of agar dissolved in physiological saline (g/l): NaCl (8.53), KCl (0.22), MgSO4·7H2O (0.25), CaCl2·2H2O (0.19). The fish recovered from the surgical operation in 25 l aquaria at 18°C with physiological saline as the aquatic medium. The aquaria bottoms were made of glass and not covered with gravel. Fish that had been subjected to corresponding types of treatments were grouped and placed in one of three aquaria. Fish were fed commercial salmon food pellets (EWOS 5A, Vextra) daily. Fish in all three aquaria swam to the place where pellets were introduced and started to snap at the food. During the week when observations of their behaviour were made, half of the physiological saline in the aquaria was replaced every day 3 h before trials.
Preparation of food extract
Salmon food pellets were suspended in physiological saline and mixed in a magnetic stirrer for 15 min. About 15% of the pellet dry weight was water soluble. The extract was filtered and injected into the aquaria at a concentration of 1.5 g dry weight of the water-soluble material per litre.
Analysis of behaviour
The different behaviour patterns of the fish were scored during 2 min periods when the fish were exposed to: (i) physiological saline or (ii) food extract. In total, 2 x 7 injections were made for each group of fish. Odorant stimuli were added to the aquaria via a polyethylene tube connected to a peristaltic pump with a flow rate of 5 ml/min for a duration of 2 min. When homogeneously distributed, the concentration of food odour in the aquarium would represent a 2500 times dilution of the introduced samples, i.e. 0.6 mg/l. The behaviour of the fish during the experiments was recorded by a video camera. Observations were made once every day for 7 days starting 1 week after the surgery. Total observation time for each group of fish was 28 min. The observer was not informed about the treatment of the different groups of fish.
The behaviours were scored from video recordings, which were repeated to follow the behaviour of each and every fish throughout the 2 min injection time. The following classes of feeding behaviours were scored: biting against the bottom, walls or congeners; snapping, a fast movement with the jaws at objects on the bottom or in mid-water or at the outlet of the plastic tube used for injecting substances; mouth opening, slow movements of the jaws in mid-water; vertical posture, where the fish were grasping objects on the bottom at an angle close to 90° to the bottom.
In addition to these behaviours, we saw other types of activity which could be interpreted as exploratory or search behaviour. Thus we observed the following behavioural parameters: activation, swimming downward, searching and location of the tube outlet. These behaviours were noted as present, questionable or not present for each of the seven sessions of the 2 min injection periods (Table 1).
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The means and standard deviations are given for the biting, snapping, mouth openings and vertical posture behaviours (Table 1). To compare the different treatments, the scores for the four classes of behaviour patterns were pooled and two-tailed t-tests with different variance were made (Table 2).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Behaviour during injection of physiological saline
Control and LOT-intact fish
The fish in these two aquaria swam slowly around in the middle or lower
water layers, or they stood still for several minutes. These fish rarely
snapped, or bit the walls or their congeners, and bottom food search with a
vertical posture was not observed. During the 2 min period encompassing the
injection of physiological saline into the tank, the scores related to feeding
were low, and activation, swimming downward, searching and location of the
tube outlet were seldom seen (Table
1).
LOT cut
The fish with the LOT cut and the mMOT and lMOT intact had initially darker
skin coloration than fish of the other groups. The fish were quiet and stood
still for hours in the same place. Biting or snapping happened very rarely.
Food search behaviour was never seen. During the 2 min period of physiological
saline injection the scores were low for all types of behaviour patterns
(Table 1).
Behaviour during injection of food odour
Control and LOT-intact fish
The injections of food extract evoked typical food search behaviour both in
control fish and fish with the LOT intact
(Table 1). The first signs of
an evoked reaction were mouth openings in mid-water, in which there were often
4-6 mouth openings in rapid sequence. The fish then dove towards the bottom of
the tank and started to bite the bottom or walls of the aquarium. In several
trials, the fish bit their congeners. The fish swam rapidly around in the
aquarium and after 1 min gathered around the outlet of the injection tube,
biting frequently. Several times during the 2 min injection period the fish
adopted a vertical posture, snapping at the bottom. Occasionally, fish swam
for short periods to the surface, only to return to the bottom, snapping at
particles in the water.
One control fish did not show any signs of feeding behaviour and stood quietly near the surface. Post-mortem inspection of the brain revealed that the blood supply to the olfactory bulbs of this fish was impaired. This feature might explain the lower scores for the control fish than the fish with the LOT intact. The olfactory system in the other control fish was intact. The fish group with LOT intact had a normal blood supply to the olfactory bulbs and the interruption of the lMOT and mMOT could be confirmed.
LOT cut
The behaviour of the fish with the LOT cut was dramatically different from
the other groups of fish. Injection of food extract did not induce any
particular behaviour. The fish remained quiet and stood at the same place even
if that happened to be close to the outlet of the injection tube. These fish
did not show any signs of increased activity and snapping was never observed
(Table 1). A slight increase in
biting frequency was, however, observed in two of the seven trials. It should
be noted that in these two cases the fish stayed close to the outlet of the
injection tube.
Post-mortem inspection of the brain revealed that the blood supply to the olfactory bulbs of these fish was patent and that the lMOT and mMOT were intact. The LOTs that were cut had not regenerated.
Comparisons between the different treatments
Statistical analysis showed that there was no significant difference in feeding behaviour between the control and the LOT-intact fish (Table 2). This observation held true when injecting the physiological saline into the tank and when food extract was injected into the tank. On the other hand, those fish with the LOT cut had lower behavioural scores during the 2 min control period with the injection of physiological saline than the other two groups of fish. When injecting the food extract, the fish with the LOT cut had a highly significant lower score than the other two groups of fish. Comparing the 2 min periods of the injection of physiological saline and injection of food extract revealed significant differences for both the control fish and the fish with the LOT intact. However, there was no significant difference between these same treatments for the fish with the LOT cut, thus confirming the loss of sensitivity.
These results clearly show that the fish with the LOT cut displayed a drastically lower number of food search behaviours. Furthermore, the fish with only the LOT intact had the same behavioural scores as the control fish. In other words, the fish with the LOT cut had lost their ability to react to food odours.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The results of the present study demonstrate striking differences in behaviour between the fish with LOT intact and those with LOT cut, suggesting that, in the absence of visual and tactile stimuli, the LOT is necessary to maintain the full qualitative and quantitative extent of feeding behaviour in crucian carp via the olfactory organ. This is not to say that all behaviour patterns that can be related to feeding are absent when the LOT is cut. Crucian carp with the LOT cut can respond to the presence of food pellets, and some reaction patterns could be observed in the absence of any discernible stimuli. It is also worth noting that food extract induced a slight increase in the frequency of biting among the fish with LOT cut; however, the behavioural patterns of mouth opening, snapping and vertical posture did not change upon injection of food extract. Biting is associated with feeding, but can also be part of aggressive and search behaviour. Feeding behaviour may also be evoked by the other chemsosensory systems (Kotrschal, 2000
), which were
intact in our experimental fish.
In two instances we saw feeding behaviour in the LOT-cut fish. These were
observed when the fish happened to be close to the outlet of the injection
tube; it seems possible that in these instances the concentration of food
odour was sufficiently high to induce food search behaviour via the extraoral
taste system. Taste buds are abundant (82-162 mm-2) in the gular,
forehead and operculum area in crucian carp
(Gomahr et al.,
1992). It has been shown that anosmic channel catfish,
Ictalurus punctatus, which have numerous external taste buds, do
respond to food odours (Bardach et
al., 1967). Both electrophysiological and behavioural studies
show that the external taste receptors are more sensitive than oral taste buds
(Kanwal and Caprio, 1988;
Kasumyan, 1999).
In behavioural trials the difference between thresholds for olfaction and
gustation is high. The threshold concentrations for the most stimulatory taste
substances are usually 10-2-10-4 M
(Hidaka, 1982;
Adams et al., 1988;
Jones, 1989;
Lamb and Finger, 1995;
Kasumyan and Morsy, 1996). The
threshold concentrations for substances that induce food search behaviour in
fish via the olfactory system are least 2-5 orders of magnitude lower
(Ellingsen and Døving,
1986; Kasumyan and Taufik,
1994). In natural waters the concentration of free amino acids
that evoke food search behaviour are of the order of
10-6-10-7 M (Poulet
and Martin-Jezequel, 1983;
Poulet et al., 1985;
Williams and Poulet, 1986).
These concentrations would evoke behavioural reaction via the olfactory but
not the gustatory system.
Another interpretation of our results is that the fibres of the MOT can
mediate feeding behaviours. Following crushing of the LOT, goldfish lost the
ability to discriminate low (10-8 M) but not high (10-6
M) concentrations of stimuli (Zippel
et al., 1993). Regeneration appeared after 2 weeks
(von Rekowski and Zippel,
1993). This recovery time is so short that one can ask if the
lesion included all fibres in the tract equally efficiently. The authors
conclude that the LOT is responsible for the discriminatory ability, whereas
similar concentrations of the rewarded and the concurrent stimuli
(10-6 M) can also be discriminated via the MOT. Stacey and Kyle
(Stacey and Kyle, 1983) stated
that both the MOT and the LOT were needed to maintain feeding responses to
food odours in goldfish. In the latter study, we speculate that post-operative
recovery time may play a role. It is worth noting that in our experiments the
period between surgical operation and behavioural trials was short and
prevented the possibility of the olfactory nerve acquiring even limited
amounts of patency or compensation by other sensory systems. This
post-operative recovery period is an important consideration in fishes as
research on the stellate sturgeon, Acipenser stellatus, demonstrated
that they could begin to respond to food odour 3 months after bilateral
cauterisation of the olfactory rosettes
(Kasumyan and Devitsina,
1997). While the sturgeon's olfactory system was impaired however,
the external gustatory system showed a peripheral proliferation and thus, to a
certain degree, had compensated for the loss of olfactory sensitivity to food
odours. We concluded that a period of 1 week is not enough for our
experimental fish to recover an ability to respond to food stimuli by using
the gustatory system.
A number of experiments using different techniques have yielded results
that support the present findings. Electrophysiological studies of the nervous
activity at the surface of the olfactory bulb of salmonids showed that the
lateral part of the bulb responded to amino acids generally thought to be food
odours, while the medial part respond to bile salts
(Thommesen, 1978;
Døving et al.,
1980). These results have been confirmed by investigations into
the bulbar responses in zebrafish (Brachydanio rerio) using
voltage-sensitive dyes coupled with stimulation with different odorants
(Friedrich and Korsching,
1997). Furthermore, amino acids evoked responses in the lateral
part of the bulb, and fish pheromones (17
,
20ß-dihydroxy-4-pregnene-3-one-20-sulphate and prostaglandin
F2) and bile salts give responses in restrict regions of the
medial olfactory bulb. Application of neural tracers to discrete regions of
the olfactory bulb revealed that sensory neurons of a particular type are
spread out in the olfactory epithelium
(Morita and Finger, 1998).
Neurons expressing specific putative olfactory receptors appear to be randomly
distributed within the sensory epithelium
(Ngai et al., 1993;
Asano-Miyoshi et al.,
2000). It is worth noting that there is a topographical projection
from the olfactory bulb to the olfactory tract in both carp, Cyprinus
carpio (Satou et al.,
1979), and tench, Tinca tinca
(Dubois-Dauphin et al.,
1980), such that the majority of neurons that are situated in the
medial part of the bulb projected to the medial tract and the majority of
neurons in the lateral part of the bulb project to the lateral tract.
These results on the olfactory system in teleosts are supported by studies
on the mammalian olfactory bulb, which have demonstrated that receptor neurons
expressing a given receptor converge onto a small number of synaptic
structures (glomeruli) in the olfactory bulb
(Ressler et al.,
1994; Vassar et al.,
1994; Mombaerts et
al., 1996). In future experiments on fish it will be
important to describe which olfactory receptors are expressed in the different
types of sensory neurons in the fish olfactory epithelium and what kind of
behaviour patterns they mediate. An advance in this direction was recently
published by Speca et al. (Speca
et al., 1999) who showed that receptor 5.24 responded to
basic amino acids. The implication of the present experiments is that sensory
neurons that express receptors tuned to food odours terminate in a specific
region of the olfactory bulb. The present study and that of Hamdani et
al. (Hamdani et al.,
2000) lay the basis for studies indicating which type of receptor
neurons make synapses with neurons projecting to the MOT and the LOT
(Hamdani et al.,
2001).
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Acknowledgments |
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The authors are grateful to Johan B. Steen and Kurt Kortschal for comments on earlier versions of this manuscript and to George Alexander for correcting the English. This study was supported by the Research Council of Norway.
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Accepted July 5, 2001
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A. A. Nikonov, T. E. Finger, and J. Caprio Beyond the olfactory bulb: An odotopic map in the forebrain PNAS, December 20, 2005; 102(51): 18688 - 18693. [Abstract] [Full Text] [PDF]
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 Y. Sato, N. Miyasaka, and Y. Yoshihara Mutually Exclusive Glomerular Innervation by Two Distinct Types of Olfactory Sensory Neurons Revealed in Transgenic Zebrafish J. Neurosci., May 18, 2005; 25(20): 4889 - 4897. [Abstract] [Full Text] [PDF]
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A. Hansen, S. H. Rolen, K. Anderson, Y. Morita, J. Caprio, and T. E. Finger Correlation between Olfactory Receptor Cell Type and Function in the Channel Catfish J. Neurosci., October 15, 2003; 23(28): 9328 - 9339. [Abstract] [Full Text] [PDF]
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F.-A. Weltzien, E. Hoglund, E. H. Hamdani, and K. B. Doving Does the Lateral Bundle of the Medial Olfactory Tract Mediate Reproductive Behavior in Male Crucian Carp? Chem Senses, May 1, 2003; 28(4): 293 - 300. [Abstract] [Full Text] [PDF]
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E. H. Hamdani and K. B. Doving Sensitivity and Selectivity of Neurons in the Medial Region of the Olfactory Bulb to Skin Extract from Conspecifics in Crucian Carp, Carassius carassius Chem Senses, March 1, 2003; 28(3): 181 - 189. [Abstract] [Full Text] [PDF]
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E. H. Hamdani and K. B. Doving The Alarm Reaction in Crucian Carp is Mediated by Olfactory Neurons with Long Dendrites Chem Senses, May 1, 2002; 27(4): 395 - 398. [Abstract] [Full Text] [PDF]
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E. H. Hamdani, G. Alexander, and K. B. Doving Projection of Sensory Neurons with Microvilli to the Lateral Olfactory Tract Indicates their Participation in Feeding Behaviour in Crucian Carp Chem Senses, November 1, 2001; 26(9): 1139 - 1144. [Abstract] [Full Text] [PDF]
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