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First published online October 31, 2008
Journal of Experimental Biology 211, 3529-3535 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018739
Single unit responses to skin odorants from conspecifics and heterospecifics in the olfactory bulb of crucian carp Carassius carassius
1 Department of Molecular Biosciences, Faculty of Mathematics and Natural
Sciences, University of Oslo, PO Box 1041, N-0316 Oslo, Norway
2 The Biotechnology Centre of Oslo, University of Oslo, PO Box 1125, N-0317
Oslo, Norway
* Author for correspondence (e-mail: stinel{at}imbv.uio.no)
Accepted 11 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: complex odors, olfactory bulb, species specificity, skin extract, alarm substances, pheromones, fright reaction, olfaction, teleost
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Lin et al., 2005). In fishes,
alarm substances from injured skin induce fright reaction (reviewed by
Chivers and Smith, 1998;
von Frisch, 1938), but the
skin also contains a multitude of other odorants. The present study concerns
the effect of different groups of odorants in skin extracts from different
fish species on single unit activity of OB neurons of crucian carp
Carassius carassius.
Sensory neurons responsive to a particular odorant are widely dispersed
within the olfactory epithelium (Ressler
et al., 1994b; Weth et al.,
1996), and their axons project to the OB, the first processing
center of olfactory input, forming synapses with a small number of secondary
neurons within glomeruli. In mammals, sensory neurons expressing a given
odorant receptor terminate at one or a few glomeruli forming a chemotopic
organization. Here, a spatial representation of sensory input occurs where
each glomerulus responds specifically to functionally related odorants
(Ressler et al., 1994a;
Vassar et al., 1994). A
similar organization of the OB is found in fishes (see
Hamdani and Døving,
2007) in which many biologically relevant odorants are known. The
chemotopy of the fish OBs has also been mapped
(Friedrich and Korsching,
1997; Hamdani and
Døving, 2003; Lastein
et al., 2006; Nikonov and
Caprio, 2001).
In many fish species, projections of secondary neurons to higher brain
centers form long olfactory tracts that are separated into distinct bundles.
Electrical stimulation of separate bundles in Atlantic cod Gadus
morhua lead to distinct behaviors
(Døving and Selset,
1980). These findings are congruent with studies in the crucian
carp where ablation of each bundle resulted in loss of a distinct behavior
(Hamdani et al., 2001;
Hamdani et al., 2000;
Weltzien et al., 2003). A
topological relation between the OB and the olfactory tract also exists in
fish (Dubois-Dauphin et al.,
1980; Satou et al.,
1979), i.e. each bundle, and each corresponding region of the OB,
is activated by functionally distinct odorant groups that mediate distinct
behaviors.
Many fish species respond to olfactory cues from injured skin of
conspecifics by performing stereotypic avoidance behavior (e.g. the fright
reaction) (von Frisch, 1938).
Injured skin from other species may cause the same response, but is usually
less effective than that from conspecifics
(Mathis and Smith, 1993;
Mirza and Chivers, 2001;
Smith, 1982). Extracts of fish
skin are commonly used to study the fright reaction, and odorants inducing
this behavior (the alarm substances) are believed to be stored in specialized
epidermal cells (Pfeiffer,
1963). In addition, skin extracts contain a multitude of other
odorants, such as amino acids and steroids
(Ali et al., 1987;
Hay et al., 1976;
Saglio and Fauconneau, 1985).
Applied as pure compounds, these odorants were shown to be involved in feeding
and sexual behavior, respectively. Usually, when exposed simultaneously with
alarm substances present in the skin, food- and sex-related stimuli do not
induce their `typical' behaviors, but to what extent they activate olfactory
neurons is unknown. However, when the fright-mediating part of the olfactory
tract is ablated, crucian carp perform feeding behavior
(Hamdani and Døving,
2000). This indicates activation of several types of neurons upon
skin extract detection.
In the present study, we stimulated the olfactory epithelium of the crucian carp with skin extracts from four species, crucian carp, common carp Cyprinus carpio, tench Tinca tinca, and bream Abramis brama while recording from single OB units. We took advantage of the clear OB chemotopy where regions responsive to food-related odorants, pheromones and alarm odorants, respectively, are reliably distinguishable. The aims were to examine neural activity induced by different types of skin odorants and to investigate how well injured conspecifics are distinguished from other species.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Twenty-two fish were initially anesthetized with benzocaine (45 mg l—1) and subsequently given an intraperitoneal injection of Saffan (alphaxalon 0.9% and alfadolone acetate 0.3%, 24 mg kg—1; Shering-Plough Animal Health, Welwyn Garden City, UK). Additional Saffan (24 mg kg—1) was injected intramuscularly when the duration of the experiment exceeded 5 h. To avoid unintended movements during the experiment, fish were wrapped in a wet cloth, adjusted in a cradle, and fixed belly down by two steel rods towards the upper parts of the orbital bones. Fish were continuously irrigated through the mouth and over the gills by city spring water during the experiments. The right olfactory tract and the right OB were exposed by removing the skull roof under a stereomicroscope. The mesenchymal tissue around the olfactory tract was aspirated by gentle use of a moist sponge, and the anterior part of the brain cavity was filled with paraffin oil. The preparation allowed recording of nervous activity for at least 8 h after the surgery.
Preparation of skin extracts
Skin was removed from previously frozen crucian carp, common carp, tench,
and bream. Approximately 2 g of skin was homogenized manually with 100 ml
distilled water in a mortar. The homogenate was filtered through glass wool
and frozen immediately at —20°C in 1 ml aliquots. Freezing does not
interfere with the functional properties of alarm substances
(Lawrence and Smith, 1989;
Stabell and Lwin, 1997). The
procedure might alter the proportions of odorants in the skin and/or cause
loss of certain odorants; however, the extracts are prepared in the same way
as to those we have used in our behavioral studies. In addition, this
substantially reduced the number of individuals needed to produce skin
extracts.
At the day of experiment the filtrates were diluted in oxygenated artificial pound water (APW) to a final concentration of 10—2 or 10—4 from the stock solutions. APW was prepared by adding the following chemicals to distilled water (mmoll—1): NaCl (0.5), KCl (0.05), CaCl2 (0.52), NaHCO3 (0.19).
Test solutions of commercial chemicals
Four test solutions were prepared for the identification of units in the
pheromone region and the food region of the OB. Solution 1: the sex pheromones
17,20β-dihydroxy-4-pregnen-3-one,
17,20β-dihydroxy-4-pregnen-3-one-20-sulfate, androstenedione, and
prostaglandin F2
(2.5x10-10 mol
l—1 each). Solution 2: the bile salts; glucocholic acid,
glucolithocholic acid, taurocholic acid, and taurolithocholic acid
(2.5x10—10 moll—1 each). Solution 3:
the amino acids glycine, L-arginine, L-proline, and
L-serine (2.5x10—5 mol l—1
each). Solution 4: the polyamine spermine (1.0x10—5 mol
l—1). All solutions were made in APW and applied in
concentrations as described above.
The sex pheromones and bile salts were separately prepared as stock solutions (600µl) at a concentration of 10—3 moll—1 in dimethyl sulfoxide. Amino acids and spermine were separately prepared as stock solutions (1 ml) at a concentration of 0.1 mol l—1 in APW. All solutions were stored at —20°C. Chemicals were purchased from Sigma-Aldrich, St Louis, MO, USA.
Stimulation of the olfactory epithelium
A polyethylene tube was placed into the right anterior naris, exposing the
olfactory epithelium to a continuous flow of APW (1.2 ml
min—1). Without changing the flow rate, the APW was replaced
by odorant solutions using miniature valves connected to the tube. This
installation minimized the risk of mechanical stimulation and prevented the
epithelium from drying. Between each exposure, a flow of APW was directed to
the olfactory epithelium to ensure that all stimulating substances were washed
out from the olfactory capsule. The olfactory epithelium was not stimulated
for a second time until the nervous activity returned to the prestimulus
level.
Single unit recordings
Nervous activity was investigated by extracellular recordings from single
OB units using microelectrodes made from tungsten wire (125 µm, impedance
1—2 M
, 1 kHz), prepared as described previously
(Hubel, 1957). The
microelectrode position was adjusted by a motorized micromanipulator (SD
Instruments MC 1000, Grant Pass, OR, USA), and the signals led to a
differential amplifier (DP 301, Warner Instrumental, Hamden, CT, USA). The
reference electrode was positioned on the border of the brain cavity. The
bandwidth was adjusted to 0.3—3 kHz, and a notch filter of 50 Hz was
activated. Signals from the amplifier were displayed on an oscilloscope
(Tektronix 565; Portland, OR, USA). The nervous activity was digitalized with
an A/D converter (µ1401; CED, Cambridge, UK), stored and later analyzed by
software (Spike 2, version 4.04; CED, Cambridge, UK).
The distance between the electrode and the neuron determines the amplitude and shape of action potentials as it appears on the computer. The Spike program allowed the sorting of action potentials based on these parameters, thereby distinguishing between different units at the same electrode position.
Experimental procedure
The alarm, the pheromone and the food regions can be reliably distinguished
in the crucian carp OB, where neurons are selectively activated by alarm
odorants, pheromones and food-related odorants, respectively
(Hamdani and Døving,
2003; Lastein et al.,
2006). Recordings were made from units in all regions upon
exposure to skin extracts. The electrode was introduced from the dorsal side,
and the position of each electrode trajectory was marked on a schematic
drawing of the OB (Fig. 1).
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Analysis of single unit activity
Units can be divided into two categories, type I and type II
(Hamdani and Døving,
2003; Zippel et al.,
2000). In brief, type I units are assumed to correspond to the
activity of mitral cells and respond with a burst of impulses concomitant with
the stimulus arriving at the olfactory epithelium. Their responses to odorants
reflect the chemotopic organization of the OB. Type II units are believed to
correspond to the activity of the ruffed cells. These neurons lack a clear
chemotopic organization found in the mitral cells (S.L. and E.H.H., personal
observation). In the present study, only type I units that responded to at
least one of the stimuli were included in the analysis. Previous studies show
that the spontaneous and the interstimulus activity of type I units varied
between 0.01 and 4 spikes s—1
(Hamdani and Døving,
2003; Zippel et al.,
2000). However, most type I units sensitive to skin extracts had a
very low spontaneous and interstimulus activity, all responding with increased
activity upon stimulation (Hamdani and
Døving, 2003).
In the present study, single unit recordings were performed to compare nervous activity induced by different stimuli. Only type I units that responded to at least one of the stimuli are included in the analysis. The effect of a skin extract was categorized as a response (+) if there was a burst of impulses, or as a no response (0). In congruence with our previous studies, no inhibitory responses were observed. The response profiles where collected in a data sheet from units in each region, and separate data sheets were made for stimuli with the high and low concentrations of the skin extracts. The ability to discriminate between the skin extracts was investigated by pair-wise comparisons. A unit was considered to discriminate between skin extracts from two different species when responding to only one of the two extracts. A unit was considered not to discriminate between skin extracts from two different species when responding to both or none.
Validation of response analysis
The burst of impulses observed upon stimulation is easily recognizable,
however, to verify that the increased activity was statistically significant,
a sub-set of 40 units was randomly chosen. The spontaneous activity was
assessed from an interstimulus time interval of 30 s, which was divided in six
periods of 5 s. The number of spikes in each period was counted and the mean
and standard deviation was calculated. These values were compared to the
number of spikes during a 5 s response period during stimulation.
The induced activity always exceeded the mean interstimulus activity, and all nervous activity considered a response was more than a multiple of 3.85 standard deviations from mean interstimulus activity (range 3.85—81.24). Thus, the measured increase in activity (burst) upon stimulation was always statistically significant (confidence interval, P<0.001). The mean interstimulus activity and the induced activity are plotted for each unit (Fig. 2).
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To ensure that these units were typical for the entire population of tested
units, a second sub-set was randomly chosen, and for the two sub-sets the
interstimulus activities were compared by a 
2-test (Microsoft
Excel 2003). The units were divided into the following intervals (in spikes
s—1); less than 0.1, 0.1—0.2, 0.2—0.3,
0.3—0.6 and more than 0.6. In sub-set 1 the frequencies ranged from
<0.03 to 1.3 spikes s—1, and in sub-set 2 from <0.03 to
1.6 spikes s—1. There was no significant difference between
these two sub-sets (2-test, P=0.59), and one sub-set
may therefore be regarded as typical for the entire population of units.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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We frequently encountered responding units at two successive electrode positions that were separated by less than 100 µm. If two or more such units evoked identical response profiles and shape of action potential, only one was kept for the subsequent analysis. In total, 104 units were discarded by this procedure. The results from the analysis of the two data sets were similar (data not shown). Also, in numerous trajectories (not shown), units were discovered as a result of their spontaneous activity, but did not respond to any of the stimuli used in the present study. These units were not included in the calculations as the aim was to investigate units responding to skin extracts.
Units responding to different skin extracts in different OB regions
The number and percentage of units responding to each skin extract is
presented for each OB region (Fig.
4). In the alarm region, the number of units activated was lower
when stimuli were applied at low concentrations compared to high
concentrations for all skin extracts except tench. Units in the pheromone
region were in general more frequently activated by the low than by the high
concentrations of skin extracts. A notable exception was the percentage of
units activated by the conspecific skin extract; which was 72.7% at the high
and 19.6% at the low concentration. Units in the food region were more
frequently activated by the high than by the low concentrations of skin
extracts. At both concentrations the conspecific skin extract activated fewer
units than those from heterospecifics.
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In general, the units discriminated better between skin extract from conspecifics and another species than between skin extracts from two heterospecifics. In the alarm and food regions this was prominent when applied at low concentrations. In the pheromone region this did not seem to be correlated to the concentration of the stimuli.
When applied at low concentrations, the units in the alarm region showed increased discrimination between the conspecific skin extract and the heterospecific skin extracts, compared with high concentration applications. This tendency was also observed for the units that discriminated between skin extracts from common carp and bream. In the pheromone region there was a reduction in discrimination between the conspecific skin extract and two heterospecific skin extracts, tench and bream, when applied at low concentrations. For the other pair-wise comparisons, increased discrimination was observed. In the food region, there was an increase in the percentage of units that discriminated between the low concentration applications compared to the high concentration applications.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Neural activation induced by various odorants present in the skin extracts
Many units were activated both by solutions of commercial chemicals and by
skin extracts in the pheromone and the food regions. According to previous
studies on the functional organization of the olfactory organ, OB units are
sensitive to specific odorants with approximately the same functions. Thus,
the induced neural activation suggests that odorants normally related to
reproduction and feeding are present in detectable amounts in the fish skin.
The detection of these odorants in skin extract might be biologically
relevant. It may be possible for an odorant to have more than one function
depending on context and/or concentration. Pheromone-like properties of amino
acids in fish skin were previously suggested
(Saglio and Blanc, 1989), but
this has never been confirmed. Steroids and bile salts are more likely to have
putative functions providing information about the injured fish. We speculate
that this is more important when detecting skin odorants from other species
than from conspecifics. Behavioral responses to dangers may be acquired by
previous experiences, enabling the association of odors from another prey fish
with predators (Brown and Smith,
1998; Chivers et al.,
2002; Darwish et al.,
2005; Ferrari et al.,
2005).
All skin extracts applied induced nervous activity in the alarm region. This could mean that these units respond to and discriminate between alarm substances from different species. The axons of neurons in the alarm region form the bundle of the olfactory tract (mMOT) which mediates the fright reaction and it is probably that these are activated by odorants inducing the behavior. We can still not say with certainty whether all the units are sensitive to alarm substances or whether some respond to other unknown odorants in the skin extracts.
Activation of OB neurons with comparable stimuli to those in the present
study, was investigated in rodents (Lin et
al., 2005), where a combination of single unit recordings and gas
chromatography (GC) was applied. Similar approaches could help identifying
potent alarm substances in fish skin. Previously, we performed a combination
of single unit recordings in the alarm region of the OB in conjunction with
high performance liquid chromatography (HPLC) analysis. This enabled us to
identify a highly potent fraction of the skin extract, probably containing the
alarm substances (Brondz et al.,
2004). Although such experimental procedures are possible, they
are hardly practical, since it is difficult to analyze the different
components detected by HPLC. Also a single HPLC run, which would be required
for each single unit recording, takes about an hour. Thus, such an approach
would be very time consuming.
The mitral cells located in the lateral part of the teleost OB are
morphologically different from those in the medial part
(Alonso et al., 1988;
Fuller et al., 2006), which
suggests physiological and functional distinctions. However, no differences
between the medial and the lateral OB units with respect to neural responses
were observed in the crucian carp. Still, different functions related to skin
extract identification cannot be excluded.
The skin extracts were taken from skin of previously frozen fish. This gives potent extracts which induce the fright reaction; however, this procedure might alter the proportions of odorants in the skin and/or cause loss of certain odorants. Nevertheless, the present method is the most suitable for studies on single unit activation and reduces the number of individuals needed for making the skin extracts, as application of fresh skin would require a new specimen of each species for each experiment.
Differences between responses to high and low skin extracts
The low concentrations of skin extracts correspond to what we commonly use
in behavioral studies with crucian carp and the single unit responses probably
reflect bulbar activation in free-swimming animals. Interestingly, both in the
food and in the pheromone regions of the OB the conspecific skin extract
activated considerably fewer units than did skin extracts from other species.
Lower sensitivity towards conspecific odorants and/or lower (sub-threshold)
content of potent odorants in conspecific skin compared to the other species
could account for these observations. However, we find it unlikely that the
sensitivity towards conspecific skin odorants is lower compared with
heterospecific skin odorants. A suppression of neural activity in OB regions
not activated by alarm substance when a stimulus is applied in relevant
concentrations could be a more reasonable possibility. Such a process was also
suggested previously (Lin et al.,
2006).
Suppressing activity in other regions of the olfactory bulb that mediate
messages not related to potential danger could reinforce the alarm signal.
This could prevent contradictory information from reaching higher brain
centers where sensory inputs are integrated, which may be advantageous.
Contrasting interactions between type I and type II units were demonstrated in
goldfish Carassius auratus
(Zippel et al., 2000) and in
crucian carp (Hamdani and Døving,
2003). Zippel and co-workers suggested that the type I units are
mitral cells and that type II units are the ruffed cells. A possible scheme
could be that the ruffed cells (type II), which are believed to lack input
from the sensory cells (Kosaka and Hama,
1979), suppress the activity of mitral cells (type I). Another
possibility is that the nervous activity, when reaching the brain, activates
centrifugal fibers. Centrifugal activity can be induced by odorants as well as
non-odorant stimuli, and may influence the activity of the secondary neurons
in the olfactory system (Døving,
1966; Døving and Gemne,
1966).
When applied in high concentration, the conspecific skin extract induced responses in a majority of the units, thus, there was no apparent modulation of activity. Stimulating the olfactory epithelium with an excessive amount of skin extract could potentially activate sensory neurons that normally are silent.
Discriminating between conspecific and heterospecific skin extracts
Paired comparisons showed that OB neurons in general had a better ability
to discriminate between skin extracts of crucian carp and another species,
than between skin extracts of two other species. Previous observations showed
that skin extracts from heterospecifics induced fright reactions with lower
intensities than skin extracts from conspecifics
(Schutz, 1956), which was
proposed to be based on differences in the chemical structure of alarm
substances; however, the present study shows that involvement of other
odorants could be significant.
The differences observed in discriminatory ability are probably related to properties of the odorant receptors, such that odorants from conspecifics activate other groups of sensory neurons than odorants from other species. There was also a surprisingly high number of single units in the alarm and the pheromone regions that were activated only by skin extract from crucian carp. Thus, the OB appears to have two sets of units sensitive to conspecific odorants, one informs about danger, the other informs about presence, but not necessarily danger.
Since conspecific skin extract was used to localize units in the alarm region we might potentially have missed units sensitive only to heterospecific skin extracts. Previous attempts to identify units with heterospecific skin extracts were, made but with little success, and none were located in trajectories without `conspecific-sensitive' units. We therefore assume that most, if not all units in the alarm region only sensitive to heterospecifics are located near units sensitive to conspecifics.
The difference between neural activation caused by the four skin extracts
indicates that several types of odorants may be used to distinguish between
the species. Several previous investigations focused on mate recognition among
fishes based on olfactory cues (McKinnon
and Liley, 1987; McLennan,
2003). For instance, female swordtails (Xiphophorus
nigrensis and X. pygmeaus) showed preference for conspecifics
based on olfactory, but not visual cues
(Decaprona and Ryan, 1990), and
a Lake Malawi cichlid fish (Pseudotropheus emmiltos) showed
preference for conspecifics only when olfactory cues were present
(Plenderleith et al., 2005).
These studies and the present findings demonstrate the central role of
olfactory cues in identification of other individuals.
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Acknowledgments |
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