Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803
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ABSTRACT |
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Nikonov, Alexander A. and
John Caprio.
Electrophysiological Evidence for a Chemotopy of Biologically
Relevant Odors in the Olfactory Bulb of the Channel Catfish.
J. Neurophysiol. 86: 1869-1876, 2001.
Extracellular electrophysiological recordings from single olfactory
bulb (OB) neurons in the channel catfish, Ictalurus
punctatus, indicated that the OB is divided into different
functional zones, each processing a specific class of biologically
relevant odor. Different OB regions responded preferentially at
slightly above threshold to either a mixture of 1) bile
salts (10-7 to 105 M
Na+ salts of taurocholic, lithocholic, and
taurolithocholic acids), 2) nucleotides
[10-6 to 10-4 M
adenosine-5'-triphosphate (ATP), inosine-5'-monophosphate
(IMP), and inosine-5'-triphosphate (ITP)], or 3)
amino acids (10-6 to
10-4M L-alanine,
L-methionine, L-arginine, and
L-glutamate). Excitatory responses to bile salts were
observed primarily in a thin, medial strip in both the dorsal (100-450
µm) and ventral (900-1,200 µm) OB. Excitatory responses to
nucleotides were obtained primarily from dorsal, caudolateral OB,
whereas excitatory responses to amino acids occurred more rostrally in
the dorsolateral OB, but continued more medially in the ventral OB. The
chemotopy within the channel catfish OB is more comparable to that
previously described by optical imaging studies in zebrafish than by
field potential studies in salmonids. The present results are
consistent with recent studies, suggesting that the specific spatial
organization of output neurons in the OB is necessary for the quality
coding/decoding of olfactory information.
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INTRODUCTION |
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Axons of olfactory receptor
neurons (ORNs) of vertebrates comprise the first cranial nerve and
project to the olfactory bulb (OB), the first processing center of
odorant information within the CNS. ORN axons terminate in OB glomeruli
where they synapse with apical dendritic projections of the
mitral/tufted neurons, the output neurons of the OB, and with
associated intrinsic bulbar neurons. The ORN projection in rodents is
to discrete glomerular regions of the OB, based primarily on the
specific molecular olfactory receptors expressed within each of the
respective ORNs (Mombaerts et al. 1996; Ressler
et al. 1994
; Vassar et al. 1994
). The projection map to the mammalian OB is a functional map relating general chemical features of the odorant structure to specific glomerular fields within
the OB (Bozza and Kauer 1998
; Cinelli et al.
1995
; Guthrie and Gall 1995
; Johnson and
Leon 2000
; Johnson et al. 1998
; Mori and
Yoshihara 1995
; Rubin and Katz 1999
;
Stewart et al. 1979
; Uchida et al. 2000
;
Xu et al. 2000
). A similar organization of ORN
projection to the insect analogue of the OB, the antennal lobe, has
recently been described in the honeybee (Galizia et al.
1998
, 1999
; Joerges et al. 1997
).
Since the organizational parameter for the ORN projection to the OB is
functional rather than anatomical (i.e., a somatotopical map),
questions arise as to the precise organization of the OB. For example,
are there different portions of the OB that process specific classes of
biologically relevant odorants? It is known that different ORNs that
express different molecular receptors which detect similar types of
odorants terminate in closer OB regions than those that express
receptors to detect chemically different types of odors (Bozza
and Kauer 1998; Buonviso and Chaput 1990
;
Friedrich and Korsching 1997
, 1998
;
Imamura et al. 1992
; Katoh et al. 1993
;
Mori et al. 1992
). Are there sharp boundaries between
these functional regions? Is the OB chemotopic map bilaterally and
dorsoventrally symmetric? Although the answers may vary depending on
the species selected and the specific odorants and their concentrations tested, most are probably based on common principles across animal phyla (Hildebrand and Shepherd 1997
). A key, however, to
understanding any sensory system is deciphering what the biologically
relevant stimuli are. Unfortunately, the olfactory capabilities of most mammals appear to be so broad that effective odorants do not fall neatly into a few chemical classes. In contrast, the olfactory system
in teleosts responds to fewer odorants, and their behavioral significance often is known. Three classes of biologically relevant odorants known for teleost fish are amino acids, nucleotides, and bile
acids (Carr 1988
; Michel et al. 1988
;
Sorensen and Caprio 1998
). Fish use olfaction to
behaviorally discriminate among odorants (Valentincic et al.
1994
) and use amino acids and nucleotides as feeding cues. Bile
acids, produced by the biliary system to function as digestive
detergents (Haslewood 1967
), are released into the water
in both urine and feces (Polkinghorne 1997
) where they
serve as potent olfactory stimuli and play a role in identification of
conspecifics, apparently functioning as nonsexual attractants (Li et al. 1995
).
Previous electrophysiological (Døving et al. 1980;
Hara and Zhang 1996
, 1998
;
Thommesen 1978
) and optical imaging (Friedrich and Korsching 1997
, 1998
) investigations in
salmonids and zebrafish, respectively, were consistent in indicating a
coarse chemotopic organization in the OB for biologically relevant
odorants. Electroencephalographic (EEG) recordings, which are the
summed field potentials from an undefined volume of OB, were the sole
source of the electrophysiological evidence for OB chemotopy in
salmonids. It is, however, unknown as to what percentage of the
underlying individual bulbar neurons reflected the identical odorant
specificity of the gross EEG signal (i.e., within a particular bulbar
region were there neurons with selectivities different from that
observed in the integrated EEG signal?). Also, the calcium- and
voltage-imaging studies in the zebrafish were able to clearly visualize
only portions of the ventral OB with respect to identifying functional
regions. The present electrophysiological evidence for chemotopy in the
OB of the channel catfish is derived primarily from single-unit
analysis of the responses of neurons located throughout the OB of the
channel catfish.
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METHODS |
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Experimental animals
Channel catfish, Ictalurus punctatus (15-20 cm total
length), obtained from a local hatchery, were maintained in floating cages held in ponds at the Louisiana State University Aquaculture Center facility. The fish were fed weekly with floating commercial fish
chow. Each week catfish were transferred to an aerated, 250-l polyethylene aquarium filled with charcoal-filtered city tap water (CFTW) at the Louisiana State University Animal Care Facility and
maintained on a 12:12 light/dark regime. The temperature was held above
27°C during the spring and summer and below 20°C during the fall
and winter to inhibit growth of the pathogenic bacterium, Edwardsiella ictaluri, which causes enteric septicemia and
destroys chemosensory epithelia (Morrison and Plumb
1993). The fish were used experimentally within a 1-wk holding
time and were not fed during this period.
Animal immobilization and anesthesia
The preparation of the animals was the same as that previously
described (Kang and Caprio 1991). Each catfish was
initially immobilized with an intramuscular injection of the
neuromuscular blocking agent, gallamine triethiodide (Flaxedil; 0.03 mg/100 g). During the experiments, additional injections were applied as needed via a hypodermic needle embedded in the flank musculature. The immobilized fish was wrapped in a wet Kim-Wipe, placed into a
Plexiglas container, and stabilized using a pair of orbital ridge
clamps. The gills were irrigated using an orally inserted glass tube
supplying a constant flow of aerated, CFTW that initially contained the
anesthetic, 50 mg/l MS-222 (ethyl-m-aminobenzoate methane sulfonic
acid). Surgical wounds were also bathed with 3% tetracaine. Once
surgery was completed, the gill irrigation water was replaced with CFTW
not containing MS-222.
Surgical preparation
Access to the olfactory organ was achieved by removing skin and connective tissue between the incurrent and excurrent nares, superficial to the olfactory organ. The pedunculated OB was also exposed by removing an approximate 1-cm section of skin and subcutaneous fat at the midline of the fish caudal to the nasal capsule. Following the removal of the underlying bone and cartilage, suction was applied to remove adipose tissue from the cranial cavity, and the open space was filled with freshwater teleost Ringer solution.
Odorant stimuli and delivery
The chemical stimuli (amino acids, bile salts, and nucleotides)
were obtained commercially (Sigma Chemical) and were the purest available. Stock solutions (10-3 M) of a
quaternary mixture of representatives of four different classes of
amino acids {L-Na+glutamate
(acidic), L-arginine (basic), L-methionine
[neutral with a long side-chain (LCN)], and L-alanine
[neutral with a short side-chain (SCN)]} that were previously shown
(Kang and Caprio 1997) to be potent stimuli to ORNs of
channel catfish were prepared weekly in CFTW; log step dilutions in
CFTW to 10-6 M were made daily. Stock solutions
(10-2 M) of a ternary mixture of nucleotides
previously shown to be stimulatory to ORNs of channel catfish
(Michel et al. 1988
) [adenosine-5'-triphosphate (ATP),
inosine-5'-triphosphate (ITP), and inosine-5'-monophosphate (IMP)] dissolved in CFTW were prepared individually; 1 ml of
each stock solution was placed into cryovials and frozen at
20°C. Log step dilutions of nucleotides to 10
6 M in
CFTW were made daily. Stock solutions (10-4 M)
of a ternary mixture of bile salts [Na+ salts of
taurocholic (TCA), taurolithocholic (TLC), and lithocholic (LCA) were
prepared weekly. TLC and LCA were indicated to activate ORNs of catfish
(P. W. Sorensen, unpublished observations); TCA was also included
due to its known stimulatory action on ORNs in goldfish. TCA and TLC
(both water soluble) were prepared weekly, and log step dilutions to
10-7 M in CFTW were made daily;
10-3 M LCA was prepared in ethanol weekly, and
log step dilutions in CFTW were made daily. The concentration of
methanol to water was <1:10,000, below the olfactory threshold for
this compound (Sorensen et al. 1990
). Control solutions
included: 1) CFTW obtained from the same water source as
that used to prepare the test solutions and 2) ethanol at
the appropriate dilution for testing LCA. Interstimulus intervals were
at least 2.5 min.
Stimulus delivery was via a "gravity-feed" system employing a
spring-loaded valve (model 5301, Rheodyne, Cotati, CA) driven by a
pneumatic actuator (Model 5300) at 40 psi. Stimulus solutions and the
CFTW used to bathe the olfactory mucosa between stimuli were delivered
through separate Teflon tubes (0.79 mm diam) at a rate of 6-8 ml/min.
The olfactory cavity was continuously perfused with CFTW to
1) facilitate stimulus delivery, 2) protect the
mucosa from desiccation, 3) avoid the introduction of
mechanical artifacts associated with stimulus presentation, and
4) thoroughly rinse the olfactory cavity between stimuli (3- to 5-min interstimulus intervals). A foot switch connected to an
electronic timer (model 645, GraLab Instruments Division, Dimco-Gray,
Centerville, OH) triggered the valve to introduce the odorants for a
5-s stimulus duration. without a change in either pressure or
temperature and without dilution (Sveinsson and Hara
1990).
Recording techniques
ELECTROOLFACTOGRAM (EOG).
The underwater EOG is an odorant-induced, slow negative potential
measured in the water immediately above the olfactory mucosa that is
thought to reflect summated olfactory receptor generator potentials
(Caprio 1995; Ottoson 1971
). The EOG was
recorded in vivo with calomel electrodes via Ringer-agar-filled
capillary pipettes as reported previously (Silver et al.
1976
). The EOG signal was amplified (Grass P-18 dc amplifier),
printed on a chart recorder, digitized, and stored on a video channel
of a hi-fi VCR recorder. The EOG signal served as an indicator of both
the viability of the preparation and the response onset to the tested odorants.
OLFACTORY BULB UNIT RECORDINGS.
Unit/few unit activity (generally 350- to 1,000-µV peak-to-peak
amplitude) was recorded extracellularly from the medial, middle, and
lateral portions of the rostral, intermediate, and caudal portions of
the dorsal and ventral OB (generally 3-3.5 mm in length and 1.8-2.0
mm in width at its mid-region). Each of these nine bulbar regions was
approximately 600-700 µm in width and 800-1,000 µm in length,
depending on the size of the fish. The electrode, a low-impedance (2-5
M) platinum and gold-plated, metal-filled, glass micropipette (glass
tip, 2 µm; ball diameter, 3-4 µm), was mounted on a hydraulic
microdrive attached to a stereotaxic micromanipulator and advanced
vertically downward from the dorsal surface of the OB. Stereotaxic
methods were utilized in identifying the exact x, y
positions of each recording position in the OB (Fig.
1). The z-position (depth) of
the recording electrode was determined in micrometers directly from the
scale on the hydraulic microdrive. The zero position for the
z-axis was the point of contact of the electrode to the
surface of the OB. Due to slight variations in the dimensions of the
olfactory bulb across the different specimens tested, the position of
each vertical electrode track was converted into relative units of % total length (x-axis) and % total width (y-axis). The z-axis total length was not
determined due to the difficulty in obtaining an accurate measurement
of the dorsoventral axis of the OB in vivo. Vertical
(z-axis) electrode tracks were spaced 150 µm apart. During
a single electrode penetration, the recording electrode often
encountered regions of unit activity twice: once in the dorsal and once
in the ventral OB. The majority of recordings of OB were obtained at
primarily two ranges of depth, 150-400 µm and 700-1,000 µm where
the cell bodies and dendrites of mitral cells are located in catfish
(J. Kang and J. Caprio, unpublished observations). Units observed above
500-µm depth were defined to be within the dorsal bulb, while those
below that depth were defined as within the ventral bulb. Odor
application began once a spontaneously active unit was encountered and
was clearly isolated by fine-positioning the recording electrode via
the remote fluid-filled microdrive. For each unit, each of the three
odor mixtures (amino acids, nucleotides, bile salts) at each tested concentration was applied at least twice to the olfactory organ with at
least a 2-min interstimulus interval. Initially, a moderate concentration of each of the three odor mixtures was tested
(10-5 M amino acids, 10-6
M bile salts, 10-5 M nucleotides). For any odor
mixture that resulted in an apparent increase in activity, a log unit
lower concentration was also tested. If no apparent change in unit
activity occurred to any of the moderate concentrations of the odor
mixtures, a log unit higher concentration of the respective odor
mixture was tested. On the average, 3 to 4 bulb units were obtained
from each of 37 fish tested; at the upper extreme, 8 units were
recorded in each of 2 fish. The neural activity was amplified (Grass
Instruments P511k; band-pass 30-10,000 Hz), observed with an
oscilloscope, digitized, and stored on a video channel of a hi-fi VCR.
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DATA ACQUISITION AND ANALYSIS. All recorded data from both the olfactory lamellae and OB were digitized at 32 kHz and analyzed off-line by Discovery software (Brainwave Systems Discovery package Version 5.0 with Autocut, DataWave Technologies, Longmont, CO) and printed. Some of the waveform parameters that were utilized by the software to identify and discriminate extracellularly recorded action potentials were peak amplitude, valley amplitude, spike height, spike width, spike time, and time between spikes. Spike events, EOG signals, and experimental parameters (i.e., beginning of a recording period, onset of stimulation, and end of the recording period) were time-stamped with a 32-bit 100-µs resolution value and saved in a data file. The data files were displayed on a computer screen and viewed by Neuroexplorer (Nex Technologies, Lexington, MA) software.
Responses of single OB neurons to each of the three odor mixtures were classified as excitatory, suppressive, or null based on the interrupted time-series analysis (Crosbie 1993 ![]() |
RESULTS |
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A total of 178 single OB neurons were excited by at least one of the three (amino acid, bile salt, nucleotide) solutions tested (Fig. 2). The vast majority [156 of 178 (88%)] of the neurons sampled were excited by only one of the three stimulus mixtures that were representative of the three different classes of odorants. Forty (93%) of 43 of the nucleotide-responsive OB neurons were excited solely by the nucleotide mixture and were located within a dorsal, caudolateral region of the OB; an additional three OB neurons in this region responded excitedly to all three odorant mixtures (Figs. 3A and 4). Fifty-five (90%) of 61 bile salt-responsive OB neurons were excited solely by the bile salt mixture and were located within a medial strip that extended the length of the OB both dorsally and ventrally; three additional neurons responded excitedly also to the amino acid mixure, and three other neurons responded to all three odorant mixtures (Figs. 3, A-C, and 4). Sixty-one (82%) of 74 amino acid-responsive OB neurons were excited solely by the amino acid mixture and were located lateral to the bile salt region in more rostral and intermediate OB regions both dorsally and ventrally; five additional neurons responded excitedly also to the bile salt mixture, and four other neurons responded excitedly also to the nucleotide mixture. Four additional neurons responded to all three odorant mixtures (Figs. 3, A-C, and 4).
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DISCUSSION |
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The olfactory system of fishes responds to and distinguishes among
a variety of biologically relevant stimuli, such as amino acids,
nucleotides, and bile salts (Li and Sorensen 1997;
Marui and Caprio 1992
; Michel et al.
1988
; Sola and Tosi 1993
; Sorensen and
Caprio 1998
; Valentincic et al. 1994
). Amino
acids and nucleotides are feeding cues, whereas bile salts play a role
in identification of conspecifics, apparently functioning as nonsexual
attractants (Li et al. 1995
). Each of these families of
biologically relevant stimuli are detected via different molecular
olfactory receptors (ORs) (Bruch and Rulli 1988
;
Caprio and Byrd 1984
; Li and Sorensen 1997
; Michel et al. 1988
), which are broadly
distributed in ORNs spread across sensory regions of the olfactory
organ (Baier et al. 1994
; Chang and Caprio
1996
; Ngai et al. 1993
; Vogt et al. 1995
). ORNs expressing the same ORs are, however, excluded from close apposition (i.e., "near neighbor exclusion" of "like"
ORNs) to each other (Baier et al. 1994
).
In direct contrast to a random or at least a broad dispersal of ORNs
expressing "like" ORs across the sensory epithelium in fish, odor
representation within the OB, which contains neural circuitry
fundamentally similar to that of mammals (Kosaka and Hama
1982), is chemotopically organized. On their course to the OB,
axons of ORNs remain parallel to the long axis of the nerve until being
redistributed by extensive sorting as they enter the OB (Riddle
and Oakley 1992
). This axon sorting is consistent with anatomical findings in rodents showing that ORNs expressing similar ORs
project to the same glomeruli within the OB (Ressler et al. 1994
; Vassar et al. 1994
) and support anatomical
(Guthrie and Gall 1995
; Guthrie et al.
1993
; Jourdan et al. 1980
; Onoda
1992
; Sharp et al. 1975
; Stewart et al.
1979
) and physiological (Buonviso and Chaput
1990
; Mori and Yoshihara 1995
; Uchida et
al. 2000
) studies indicating that glomeruli, which receive
input mostly from ORNs expressing a common OR (e.g., Vassar et
al. 1994
), are the primary coding units for odorant discrimination.
The present report, which is the first study using single-unit electrophysiology to define OB chemotopy in a teleost, indicates that the OB in the channel catfish is divided into different functional zones, each processing a specific class of biologically relevant odor. Different OB regions responded excitedly and preferentially at slightly above threshold to either a mixture of bile salts, nucleotides, or amino acids. Excitatory responses to bile salts were observed primarily in a thin, medial strip in both the dorsal (100-450 µm) and ventral (900-1,200 µm) OB. Excitatory responses to nucleotides were obtained primarily from dorsal, caudolateral OB, whereas excitatory responses to amino acids occurred more rostrally in the dorsolateral OB, but continued more medially in the ventral OB.
Although analyses of bulbar EEG responses from salmonid OBs and
calcium- and voltage-sensitive dye imaging of the zebrafish OB were
generally consistent with the present findings in channel catfish of a
mediolateral distinction on OB responsiveness, some variations were
evident. The bulbar chemotopy observed in the channel catfish (family
siluriformes) is more similar to that previously described for
zebrafish (family cypriniformes) (Friedrich and Korsching
1997, 1998
) than indicated for salmonids (family salmoniformes) (Døving et al. 1980
; Hara and
Zhang 1996
, 1998
; Thommesen
1978
). EEG recordings from the surface of the OB in salmonids,
char (Salvelinus alpinus), trout (Salmo trutta),
and grayling (Thymallus thymallus), indicated that bulbar
neurons located primarily rostrolaterally responded with increased EEG activity to amino acids, and those mainly dorsomedial responded to bile
acids (Døving et al. 1980
). A more recent EEG study
with six different species of salmonids [rainbow trout
(Oncorhynchyus mykiss), Atlantic salmon (Salmo
salar), Arctic char (Salvelinus alpinus), lake
whitefish (Coregonus clupeaformis), brown trout (Salmo
trutta), and lake char (Salvelinus namaycush)], where
electrode bulbar positions included both surface and depth recordings,
showed that responses to amino acids were most evident in the
lateral-posterior OB, which is larger caudally and becomes smaller and
more ventral rostrally. Responses to a bile acid (taurocholic acid),
however, were centered in a narrow triangular surface area in the
central region forming a thin sheet across the mid-OB over that of the amino acid-responsive region (Hara and Zhang 1998
).
This latter result concerning the more responsive bile acid region in
salmonids is the most disparate on comparison with the bulbar
chemotopic maps of zebrafish and rainbow trout. In both zebrafish and
rainbow trout, the bile acid/salt region was localized to a medial OB region. Unfortunately, nucleotides were not tested in the salmonid studies.
For zebrafish, both calcium- (Friedrich and Korsching
1997) and voltage- (Friedrich and Korsching
1998
) sensitive dye studies of responses of ORN terminals in
the OB were consistent in identifying specific subregions of the OB
that were preferentially activated by the different classes of
biologically relevant odors. In results that were more consistent with
the catfish than salmonid OB maps, both studies in zebrafish identified
a rostrolateral OB region that was primarily responsive to amino acids;
in addition, voltage-sensitive dyes indicated a primarily
anterior-medial OB region responsive to bile acids and a caudolateral
OB region responsive to nucleotides that overlapped with the posterior
portion of the amino acid-responsive region. A shortcoming of
visualizing activity of both dyes was that these studies were performed
in an explant preparation of the olfactory organ and bulb and viewed
ventrally; thus dorsal OB regions where neurons most activated by bile
acids could not be resolved. The present electrophysiological study in
the channel catfish, where unit responses of neurons in both the dorsal
and ventral OB were accessible and were recorded were generally
consistent with the optical studies in zebrafish and provided a clearer
picture of the chemotopy of the dorsal OB.
The medial-lateral distinction in chemotopy (i.e., medial, bile salts;
lateral, amino acids and nucleotides) in the OBs of channel catfish
(present report), salmonids (Hara and Zhang 1998), and
zebrafish (Friedrich and Korsching 1998
) is consistent
with mitral cell axons of the medial and lateral OB, respectively, projecting into the medial and lateral olfactory tracts
(Dubois-Dauphin et al. 1980
; Satou 1990
;
Sheldon 1912
). The neuronal activities on one side of
the fish OB are not influenced much by those in the opposite side and
may be explained by limited dendritic fields of neurons in each part of
the bulb (Satou 1990
). In this respect, only the medial
tract transmits pheromone information (Demski and Dulka
1984
; Døving et al. 1980
; Hamdani et al.
2000
; Kyle et al. 1987
; Sorensen et al.
1991
; Stacey and Kyle 1983
), whereas the lateral
tract processes food-related odors (Døving et al. 1980
;
Stacey and Kyle 1983
; Von Rekowski and Zippel
1993
). These results of medial-lateral differences in bulbar
unit specificities of teleosts to odorants are consistent with similar
findings in mammals (Bozza and Kauer 1998
;
Imamura et al. 1992
; Johnson and Leon
2000
; Mori et al. 1992
; Uchida et al.
2000
).
The presumable function of the OB chemotopic map in the channel catfish
is to enhance both the detection and discrimination of amino acids,
bile salts, and nucleotides, respectively (Xu et al.
2000). In addition, it is likely that a finer map exists within
each of the described OB functional zones for biologically relevant
odorants for each of the three classes of stimuli; i.e., the response
specificity of individual glomerular modules (Friedrich and
Korsching 1998
), and thus the individual neuronal elements within each respective zone can have different excitatory molecular receptive ranges (EMRR) (Mori and Yoshihara 1995
). For
example, with respect to the amino acid zone, single OB neurons
residing within the amino acid zone can be excited by
L-arginine (a basic amino acid) and either inhibited or
nonresponsive to L-methionine (a neutral amino acid) and
vice versa (unpublished observations). As proposed for mammals
(Mori and Yoshihara 1995
; Xu et al. 2000
; Yokoi et al. 1995
), the chemotopic organization of the
OB minimizes the distance for lateral inhibitory bulbar circuitry,
which is hypothesized to enhance contrasts in response specificity,
thus sharpening the molecular receptive ranges of the olfactory inputs to the respective glomeruli. It is known for ictalurid catfish that the
olfactory and not the taste system is required for the behavioral
discrimination of amino acids (Valentincic et al. 1994
, 2000a
,b
).
The map of chemotopy in the OB of the channel catfish (Fig. 4) is a
schematic and not an absolute map. The designated portions of the OB
that process amino acid, nucleotide, and bile salt odorants, respectively, represent the boundaries in which the OB units of different specificities were recorded. However, in addition to the
three previous classes of odorant chemicals, fish are known to detect
through olfaction pheromones, such as gonadal steroids and
prostoglandins (Sorensen and Caprio 1998); these
specific compounds, however, have yet to be identified for channel
catfish. It is also probable that additional classes of chemicals may
be found to be olfactory stimuli in fish. Thus, if additional classes of odorants are identified for the channel catfish, the bulbar chemotopic map described herein is likely to be modified. Further, although this report indicates that the spatial bulbar map is important
for the quality coding of odorant information in the channel catfish,
it does not address the role of precise timing of neural activity. It
is reasonable to assume that temporal firing patterns of neurons within
each of the three defined chemotopic regions might be important for a
finer discrimination and identification of the specific members of each
of the three major odorant classes tested here. The present results,
however, do argue that the initial stage of odorant quality coding
occurring within the OB is based on a spatial pattern of glomerular activation.
A key question is whether specific anatomical types of ORNs project to
the presently defined specialized bulbar regions. Recent findings
indicate that morphologically different types of ORNs (i.e., ciliated
and microvillous) are intermingled in the olfactory epithelium of fish
(Morita and Finger 1998) and other vertebrates (Miller et al. 1995
; Moran et al. 1982
;
Morrison and Costanzo 1990
, 1992
;
Rowley et al. 1989
) and project to different regions of
the OB. Future studies will explore whether the ciliated and microvillous ORNs, respectively, project primarily to any of the presently described chemotopic bulbar regions and thus respond preferentially to a specific class (or classes) of biologically relevant odor(s).
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ACKNOWLEDGMENTS |
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This research was supported by National Institute on Deafness and Other Communication Disorders Grant DC-03792.
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FOOTNOTES |
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Address for reprint requests: J. Caprio (E-mail: jcap{at}lsu.edu).
Received 22 January 2001; accepted in final form 11 June 2001.
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REFERENCES |
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