Electrophysiological Evidence for a Chemotopy of Biologically Relevant Odors in the Olfactory Bulb of the Channel Catfish

2001 ◽  
Vol 86 (4) ◽  
pp. 1869-1876 ◽  
Author(s):  
Alexander A. Nikonov ◽  
John Caprio

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 10−5 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, andl-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.

1995 ◽  
Vol 74 (4) ◽  
pp. 1435-1443 ◽  
Author(s):  
J. Kang ◽  
J. Caprio

1. For the first time in any vertebrate, responses of single olfactory bulb neurons to odorant mixtures were studied quantitatively in the channel catfish, Ictalurus punctatus. 2. Extracellular electrophysiological responses of 61 single olfactory bulb neurons from 36 channel catfish to binary mixtures of amino acids and to their components were recorded simultaneously with the electro-olfactogram (EOG). Tested were a total of 297 mixture trials consisting of 18 different stimulus pairs formed from 8 amino acids. 3. For 42% (126 of the 297) of the tests, no significant change (N) from spontaneous activity occurred. Responses to the remaining 171 tests of binary mixtures were excitatory (E; 29%) or suppressive (S; 29%). No response type was associated with any specific mixture across the neurons sampled. 4. Mixture interactions that changed response types (E or S) from those observed to the individual components were rare, because 89% of the responses of single olfactory bulb neurons to the tested binary mixtures were classified similarly as the responses to at least one of the components. 5. Responses of single olfactory bulb neurons were generally predictable for binary mixtures whose component responses were classified as both E, both S, and both N. For binary mixtures whose component responses were classified differently (e.g., one component evoked excitatory responses and the other evoked suppressive responses), the predictability of the response was dependent on the specific mixture type.


2007 ◽  
Vol 97 (6) ◽  
pp. 4058-4068 ◽  
Author(s):  
S. H. Rolen ◽  
J. Caprio

A chemotopic map of biologically relevant odorants (that include amino acids, bile salts, and nucleotides) exists in the olfactory bulb (OB) of channel catfish, Ictalurus punctatus. Neurons processing bile salt odorant information lie medially within this OB map; however, information as to how single neurons process bile salt odorant information is lacking. In the present report, recordings were obtained from 51 OB neurons from 30 channel catfish to determine the excitatory molecular receptive range (EMRR) of bile salt responsive neurons. All recordings were performed in vivo within the medial portions of the OB using extracellular electrophysiological techniques. Excitatory thresholds to bile salts typically ranged between 0.1 and 10 μM. The bile salt specificity of OB neurons were divided into three groups: neurons excited by taurine-conjugated bile salts only (group T), neurons excited by nonconjugated bile salts only (group N), and neurons excited by at least one member of each of the three classes of bile salts tested (group G). In addition to the conjugating group at C24 of the side-chain, OB neurons discriminated bile salts by the molecular features present at three other carbon positions (C3, C7, and C12) along the steroid backbone. These data suggest that OB neurons are selectively excited by combinations of molecular features found on the side-chain and along the steroid nucleus of bile salt molecules.


1995 ◽  
Vol 74 (4) ◽  
pp. 1421-1434 ◽  
Author(s):  
J. Kang ◽  
J. Caprio

1. Responses of 89 single olfactory bulb neurons from 43 channel catfish, Ictalurus punctatus, to amino acid odorants were recorded in vivo simultaneously with the electro-olfactogram (EOG). Recording time for individual neurons ranged from 16 to 344 min. The averaged spontaneous frequency ranged from x003C; 1 to 16 action potentials/s with a mean frequency of 5.2 +/- 3.6 (SD) action potentials/s. 2. Histological examinations of carbocyanine dye 1,1'diocadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI)-labeled olfactory bulbs and electrical stimulation of the olfactory tracts in a subset of experiments suggested that the majority of the recorded olfactory bulb neurons in this study were mitral cells. 3. Olfactory bulb neurons responded to amino acids with either an excitation or suppression of the background neural activity. Of the 337 stimulus applications, 28% of the responses were excitatory, and 33% were suppressive. The approximately 1:1 ratio of excitatory to suppressive responses for all stimulus applications suggests that suppressive responses also play important roles in the coding of odorant information in the channel catfish. 4. Responses of single olfactory bulb neurons were highly reproducible over time (up to 5 h). Responses to any amino acid never changed from excitation to suppression, or vice versa over time. 5. Single olfactory bulb neurons responded with excitation or suppression to more than one amino acid previously indicated to bind to independent receptors. 6. Estimated threshold concentrations for activation of an olfactory bulb neuron ranged from 10(-7) to 10(-3) M and were different from neuron to neuron for a particular stimulus and from stimulus to stimulus for a particular neuron. Responses of single olfactory bulb neurons to a given amino acid did not change from excitation to suppression, or vice versa, across different suprathreshold concentrations.


1997 ◽  
Vol 77 (1) ◽  
pp. 1-8 ◽  
Author(s):  
Jiesheng Kang ◽  
John Caprio

Kang, Jiesheng and John Caprio. In vivo response of single olfactory receptor neurons of channel catfish to binary mixtures of amino acids. J. Neurophysiol. 77: 1–8, 1997. For the first time in any vertebrate, in vivo responses of single olfactory receptor neurons to odorant mixtures were studied quantitatively. Extracellular electrophysiological response of 54 single olfactory receptor neurons from 23 channel catfish, Ictalurus punctatus, to binary mixtures of amino acids and to their components were recorded simultaneously with the electroolfactogram (EOG). For 57% (73 of 128) of the tests, no significant change (N) from spontaneous activity occurred. Responses to the remaining 55 tests of binary mixtures were excitatory (E; 13%) or suppressive (S; 30%). No response type was associated with any specific mixture across the neurons sampled. Eighty-six percent of the responses of catfish olfactory receptor neurons to binary mixtures were classifed similar to at least one of the component responses, a percentage comparable (i.e., 89%) with that observed for single olfactory bulb neurons in the same species to equivalent binary mixtures. The responses of single olfactory receptor neurons to component-similar binary mixtures (i.e., component responses were both E, both S, and both N, respectively) were generally (80% of 59 tests) classified similar to the responses to the components. For E+N and S+N binary mixtures, the N component often (66% of 58 tests) reduced or concealed (i.e., “masked”) the excitatory and suppressive responses, respectively. For the majority (6 of 11 tests) of E+S binary mixtures, null activity resulted. Responses to the remaining five tests were either excitatory ( n = 3) or suppressive ( n = 2).


1999 ◽  
Vol 82 (2) ◽  
pp. 564-569 ◽  
Author(s):  
K. Ogawa ◽  
J. Caprio

We investigated the neural processing of binary gustatory mixtures of amino acids by the facial taste system of the channel catfish, Ictalurus punctatus. In vivo electrophysiological recordings indicated that the magnitude of both integrated and single-unit facial taste responses to binary mixtures of amino acids was greatest if the components bound to independent receptor sites. Facial taste responses were obtained from 32 multiunit and 55 single taste fiber preparations to binary mixtures of amino acids whose components bind to independent taste receptor sites (group I) or to the same or highly cross-reactive taste receptor sites (group II). All component stimuli were adjusted in concentration to provide approximately equal response magnitude as determined by either the height of the integrated multiunit taste response or by the number of action potentials generated/3 s of response time/single taste fiber. The mixture discrimination index (MDI), defined as the response to the mixture divided by the average of the responses to the component stimuli, was calculated for each test of a binary mixture. MDIs of group I binary mixtures for both the integrated multiunit and single fiber data were significantly greater than those for either the control or group II binary mixtures. In a subset of multiunit recordings, the MDIs of a group I binary mixture across three log units of stimulus concentration were similar and significantly greater than those of a group II binary mixture. Analysis of the single fiber data also indicated that the MDIs of group I binary mixtures were significantly larger than those of group II binary mixtures for both alanine-best and arginine-best taste fibers; however, the MDIs of group I binary mixtures calculated from recordings from arginine-best taste fibers were significantly greater than those recorded from alanine-best taste fibers.


1995 ◽  
Vol 73 (1) ◽  
pp. 172-177 ◽  
Author(s):  
J. Kang ◽  
J. Caprio

1. We report for the first time in any teleost, a quantitative in vivo study of recordings from single olfactory receptor neurons (ORNs) in the channel catfish, Ictalurus punctatus, with odorant stimuli. 2. Responses of 69 spontaneously active single ORNs were recorded simultaneously with the electroolfactogram (EOG). Recording times ranged from 10 to 72 min per receptor cell with an average of 24 +/- 15 (SD) min/cell. The averaged spontaneous frequency ranged from < 1 to 12 action potentials/s with a mean frequency of 4.7 +/- 2.5 action potentials/s. 3. Catfish ORNs responded to the odorant stimuli (amino acids, bile salts, and ATP) with either an excitation or suppression of the background neural activity. Suppressive responses were encountered more frequently than excitatory responses, suggesting that suppressive responses also play an important role in olfactory coding. 4. Excitatory and suppressive responses to the different odorants were elicited from the same ORN, suggesting that different olfactory receptor molecules and different transduction pathways exist in the same ORN.


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