Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Processing of Odor Information in the Olfactory Bulb and Cerebral Lobes
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
Correspondence to be sent to: John Caprio, e-mail: jcap{at}lsu.edu
Key words: amino acids, bile salts, catfish, electrophysiology, nucleotides, odotopy, olfaction
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Introduction |
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 Top Introduction AcknowledgementsReferences |
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We are studying how odorant information is processed within the vertebrate central nervous system, the olfactory bulb (OB) and higher telencephalic nuclei. The experimental animal model tested in this study, the channel catfish, has an acute olfactory sense to known biologically relevant stimuli, such as amino acids, nucleotides and bile salts (Nikonov and Caprio, 2001
). Extracellular recordings from single neurons within the OB and within
the cerebral lobes (CL), the next ascending olfactory nucleus were performed in
vivo. We previously showed that olfactory receptor neural input to the OB is
odotopically organized (Nikonov and Caprio,
2001), with the lateral OB processing food-related odors (amino acids and
nucleotides) and the medial OB processing odors of more a social nature (bile salts).
Neurons processing amino acid and bile salt odors are distributed in both dorsal and
ventral OB regions, whereas neurons processing nucleotide information are localized to
the dorso-caudal OB region. Our studies of odorant specificity focuses on excitatory
responses of OB neurons located within the lateral amino acid zone of the catfish OB. Our
previous behavioral studies clearly showed that although catfish both taste and smell
amino acids, a functioning olfactory system is required for their discrimination
(Valentincic et al., 1994).
The present study is an attempt to determine the physiological basis for this
discrimination, with emphasis on amino acids as odorants. Although it was previously
documented (Kang and Caprio, 1995)
that OB neurons in channel catfish respond to amino acids, the present report
reinvestigated the amino acid selectivities of single OB units at lower stimulus
concentrations than previously tested with a larger number of amino acid odorants. The
majority of OB units recorded in the present investigation were likely mitral cells based
on the distribution of recording depths in the OB being consistent with the locations of
the majority of cell bodies of mitral cells identified previously in histological section
and the large and relatively constant amplitudes of the action potentials suggestive of
being elicited by the large mitral cells.
The specificity of 245 units located in the lateral, amino acid responsive portion of
the OB was determined. Ninety-one OB units (Group I) were highly selective for a single
type of amino acid (neutral, basic, acidic), compounds determined in previous
electrophysiological cross-adaptation (Caprio and
Byrd, 1984), amino acid mixture (Caprio et al., 1989;
Kang and Caprio, 1991) and biochemical
binding (Bruch and Rulli, 1988)
studies to bind to relatively independent olfactory receptor sites in this species. None
of the Group I units was excited by any of the other representative types of amino acids
at odorant concentrations up to and including 10–4 M. Overall,
86% of the 245 OB units tested responded to 
10–6 M amino
acids. The majority of the Group I units were excited by either L-methionine
(Met; n = 31; 34%) or L-arginine (Arg; n
= 28; 31%); units excited by either L-alanine (Ala; n
= 19; 21%) or monosodium glutamate (Glu; n = 13;
14%) were fewer. In contrast, the 154 OB units (Group II) were excited by a second
type of amino acid, but only at a 10–100x higher odorant concentration. Since
the selectivity of mitral cell responses to amino acids in zebrafish changed over 2.2 s
of the response, which resulted in a declustering of the response types observed during
the initial 500 ms of the response (Friedrich and
Laurent, 2001), we addressed the question of whether our classification of
response type based on an analysis of 3 s of response time would be significantly altered
by analyzing different portions of the response to 3 s stimulus applications. Of the 78
Group I units analyzed (i.e. those that were originally determined to be selectively
responsive to only Met, Ala, Arg or Glu over 3 s of response), 81 and 85% were
similarly classified when analyzing the first and third seconds of the responses,
respectively. The reason(s) for this discrepancy between odorant responses of bulbar
neurons in the channel catfish and zebrafish is currently unknown.
The remaining 154 (63%; Group II) of the 245 units tested had a broader
specificity than those of the Group I units, but their sensitivities to the amino acid
types were not randomly distributed (i.e. each unit type was not excited by other
particular types of amino acids). Similar to the Group I units, the more numerous of the
Group II units were those excited by 10–6 M Met (n =
83; 54%) or 10–6 M Arg (n = 46; 30%);
units excited by 10–6 M Ala (n = 21; 14%) or
Glu (n = 4; 2%) were fewer. The majority (70 of 83; 84%) of
the Group II units were excited by 10–6 M amino acid; the remaining
units responded to 10–5 M. Seventy-seven of 83 (93%) Group II
units with lowest threshold to methionine, a neutral amino acid with a long side-chain,
were also excited by Ala, a neutral amino acid with a short side-chain, but at a 10-fold
higher stimulus concentration. The converse, however, did not occur, as Group II units
with lowest thresholds to alanine were not excited by Met. This Met Group of OB neurons
showed high specificity to neutral amino acids as none of the 83 Met units were excited
by Arg or Glu. The Ala units were the least specifically tuned of the Group II OB neurons
as 86% were also excited by 10–4 M Arg and 71% by
10–4 M Glu. Although only 7% (17 of 245) of the OB units analyzed
(including Groups I and II) had the lowest thresholds to Glu, this amino acid at high
stimulus concentrations stimulated the vast majority (60 of 67 units; 90%) of two
of the other three types of Group II units.
Because of their high selectivity, we explored further the response specificity of 69 additional Group I OB units to additional amino acids and derivatives at stimulus concentrations from 10–9 to 10–5 M. An additional 31 Group I units that were excited only by Met (not by Ala, Arg or Glu) were tested with an additional eight related odorants. Two Groups emerged, those most responsive (i.e. with lowest excitatory electrophysiological thresholds) to neutral amino acids with long, linear side-chains and those with branched side-chains. Of 12 additional Group I OB units that were initially excited only by Ala (not by Met, Arg or Glu), all were most sensitive to Ala, and 5 of the 12 were equally responsive to L-serine, another neutral amino acid with a short side-chain. An additional 26 Group I OB units that were initially excited only by Arg (not by Met, Ala or Glu) were tested with eight odorants related to Arg. These units were excited by amino acids that possessed in their side-chains at least three methylene groups and a terminal amide or guanidinium group. Group I OB units that were most selective to Glu were too few to study. Overall, these collective results are sufficient to account for many of the previous results of the behavioral discrimination of amino acids in this and related species of teleosts (see Valentincic in this issue).
The second portion of this ongoing study is to determine how odorant information
arriving from the olfactory bulb via the medial and lateral olfactory tracts is
represented in the cerebral lobes (CL) of the telencephalon in the channel catfish.
Odor-responsive neurons in the CL were located in caudo-medial and lateral regions as
predicted from previous anatomical studies in catfish (Finger, 1975;
Bass, 1981). The lateral olfactory
tract (LOT) projects to the ventrolateral wall of the telencephalon and extends dorsally
and caudally in the CL, whereas the medial olfactory tract (MOT) projects medially,
rostral to the anterior commissure; however, both lateral and medial termination zones
receive input from the LOT and MOT. Although a segregation of function for olfactory
pathways in the CNS has not been studied in most animals, functional differences are
evident in fish between odorant information carried by MOT (food-related) and LOT (social
stimuli). The medial–lateral distinction in odotopy of the OB in the channel
catfish (Nikonov and Caprio, 2001) is
consistent with this distinction. The initial question of the present investigation was
to determine whether the chemotopic organization of the olfactory bulb to feeding
(lateral OB) and social (medial OB) odors is maintained, altered or eliminated at the
next ascending olfactory nucleus in the CL. A second question was whether the odorant
specificities observed in the olfactory bulb to these three classes of odorant stimuli
are maintained or altered at the next synaptic level.
Fifty-one CL neurons were excited and 22 were suppressed by odorants (amino acid or bile salt). Twenty-nine of the 35 units that were excited by amino acids were located more laterally in the CL and their odorant specificity was similar to Group I OB neurons. Sixteen units located more medially in the CL were excited by bile salts and were unresponsive to amino acids. Thus, the medial–lateral distinction between excitatory responses to bile salts and amino acids as observed in the OB is reflected in the CL; how nucleotide information is represented in the CL is currently being investigated. Further, evidence of a convergence of amino acid information that was previously separate in the OB was observed in six CL units that were excited by both neutral and basic amino acids. Ongoing studies are aimed at examining odorant specificities of CL neurons to a broader array of odorants.
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Acknowledgements |
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TopIntroductionAcknowledgementsReferences |
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Supported by NIH DC-03792 and NSF IBN-0314970.
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References |
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TopIntroductionAcknowledgementsReferences |
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Bruch, R.C. and Rulli, R.D. (1988) Ligand binding specificity of a neutral L-amino acid olfactory receptor. Comp. Biochem. Physiol. B, 91, 535–540.[CrossRef][Medline]
Caprio, J. and Byrd, R.P., Jr (1984) Electrophysiological evidence for acidic, basic and neutral amino acid olfactory receptor sites in the catfish. J. Gen. Physiol., 84, 403–422.
Caprio, J., Dudek, J. and Robinson, J.J., II (1989) Electro-olfactogram and multiunit olfactory receptor responses to binary and trinary mixtures of amino acids in the channel catfish, Ictalurus punctatus. J. Gen. Physiol., 93, 245–262.
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Friedrich, R.W. and Laurent, G. (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science, 291, 889–894.
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Kang, J. and Caprio, J. (1995) Electrophysiological responses of single olfactory bulb neurons to amino acids in the channel catfish, Ictalurus punctatus. J. Neurophysiol., 74, 1421–1434.
Nikonov, A.A. and Caprio, J. (2001) Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. J. Neurophysiol., 86, 1869–1876.
Valentincic, T., Wegert, S. and Caprio, J. (1994) Learned olfactory discrimination versus innate taste responses to amino acids in channel catfish, Ictalurus punctatus. Physiol. Behav., 55, 865–873.[CrossRef][Medline]
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