Citrate Enhances Olfactory Receptor Responses and Triggers Oscillatory Receptor Activity in the Channel Catfish

2000 ◽  
Vol 83 (5) ◽  
pp. 2676-2681 ◽  
Author(s):  
James M. Parker ◽  
Qinhui Chang ◽  
John Caprio
Keyword(s):  
Amino Acid ◽  
Binary Mixture ◽  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Olfactory Receptor ◽  
Barium Chloride ◽  
Strontium Chloride ◽  
Olfactory Responses ◽  
Receptor Neurons ◽  
High Concentrations

Citrate, a normal constituent of cellular metabolism, in a binary mixture with an amino acid enhanced asynchronous olfactory receptor responses in the channel catfish, Ictalurus punctatus. In addition, high concentrations of either citrate (≥3 mM) alone or an amino acid (≥0.1 mM) in a binary mixture with citrate (≥1 mM) triggered synchronized voltage oscillations of olfactory receptor neurons (ORNs) known as “peripheral waves” (PWs). Binary mixtures containing lower concentrations of an amino acid also triggered PW activity if the concentration of citrate in the mixture was increased. Both the enhancement of asynchronous activity and the generation of PW activity were the result of citrate chelating calcium, which lowers the surface potential of ORNs making them hyperexcitable. These effects of citrate are replicated by EGTA. Inactivation of the chelating ability of citrate and EGTA with 1 mM calcium chloride, barium chloride, or strontium chloride abolished both the enhancement of asynchronous olfactory responses and PW activity, while not affecting olfactory receptor responses to the amino acids alone.

In Vivo Responses of Single Olfactory Receptor Neurons of Channel Catfish to Binary Mixtures of Amino Acids

1997 ◽  
Vol 77 (1) ◽  
pp. 1-8 ◽  
Author(s):  
Jiesheng Kang ◽  
John Caprio
Keyword(s):  
Amino Acids ◽  
Binary Mixtures ◽  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Olfactory Receptor ◽  
Olfactory Receptor Neurons ◽  
Electrophysiological Response ◽  
Receptor Neurons ◽  
First Time

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).

In vivo responses of single olfactory receptor neurons in the channel catfish, Ictalurus punctatus

1995 ◽  
Vol 73 (1) ◽  
pp. 172-177 ◽  
Author(s):  
J. Kang ◽  
J. Caprio
Keyword(s):  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Olfactory Receptor ◽  
Action Potentials ◽  
Olfactory Receptor Neurons ◽  
Receptor Neurons ◽  
Spontaneous Frequency ◽  
Excitatory Responses ◽  
First Time

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.

scholarly journals Odorant receptors activated by amino acids in sensory neurons of the channel catfish Ictalurus punctatus.

1993 ◽  
Vol 102 (6) ◽  
pp. 1085-1105 ◽  
Author(s):  
T T Ivanova ◽  
J Caprio
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Olfactory Receptor ◽  
Action Potentials ◽  
Single Channel ◽  
Odorant Receptors ◽  
Olfactory Neurons ◽  
Whole Cell

Odorant receptors activated by amino acids were investigated with patch-clamp techniques in olfactory receptor neurons of the channel catfish, Ictalurus punctatus. The L-isomers of alanine, norvaline, arginine, and glutamate, known to act predominantly on different olfactory receptor sites, activated nondesensitizing inward currents with amplitudes of -2.5 to -280 pA in olfactory neurons voltage-clamped at membrane potentials of -72 or -82 mV. Different amino acids were shown to induce responses in the same sensory neurons; however, the amplitude and the kinetics of the observed whole cell currents differed among the stimuli and may therefore reflect activation of different amino acid receptor types or combinations of receptor types in these cells. Amino acid-induced currents appeared to have diverse voltage dependence and could also be classified according to the amplitude of the spontaneous channel fluctuations underlying the macroscopic currents. A mean single-channel conductance (gamma) of 360 fS was estimated from small noise whole-cell currents evoked by arginine within the same olfactory neuron in which a mean gamma value of 23.6 pS was estimated from 'large noise' response to norvaline. Quiescent olfactory neurons fired bursts of action potentials in response to either amino acid stimulation or application of 8-Br-cyclic GMP (100 microM), and voltage-gated channels underlying generation of action potentials were similar in these neurons. However, in whole-cell voltage-clamp, 8-Br-cyclic GMP evoked large rectangular current pulses, and single-channel conductances of 275, 220, and 110 pS were obtained from the discrete current levels. These results suggest that in addition to the cyclic nucleotide-gated transduction channels, olfactory neurons of the channel catfish possess a variety of odor receptors coupled to different types of transduction channels.

scholarly journals Electro-olfactogram and multiunit olfactory receptor responses to complex mixtures of amino acids in the channel catfish, Ictalurus punctatus.

1991 ◽  
Vol 98 (4) ◽  
pp. 699-721 ◽  
Author(s):  
J S Kang ◽  
J Caprio
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Binary Mixtures ◽  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Olfactory Receptor ◽  
Complex Mixtures ◽  
Neutral Amino Acids ◽  
Acidic Amino Acids ◽  
Receptor Sites

In vivo electrophysiological recordings from populations of olfactory receptor neurons in the channel catfish, Ictalurus punctatus, clearly showed that both electro-olfactogram and integrated neural responses of olfactory receptor cells to complex mixtures consisting of up to 10 different amino acids were predictable with knowledge of (a) the responses to the individual components in the mixture and (b) the relative independence of the respective receptor sites for the component stimuli. All amino acid stimuli used to form the various mixtures were initially adjusted in concentration to provide approximately equal response magnitudes. Olfactory receptor responses to both multimixtures and binary mixtures were recorded. Multimixtures were formed by mixing equal aliquots of 3-10 different amino acids. Binary mixtures were formed by mixing equal aliquots of two equally stimulatory solutions. Solution 1 contained either one to nine different neutral amino acids with long side-chains (LCNs) or one to five different neutral amino acids with short side-chains (SCNs). Solution 2, comprising the binary mixture, consisted of only a single stimulus, either a LCN, SCN, basic, or acidic amino acid. The increasing magnitude of the olfactory receptor responses to mixtures consisting of an increasing number of neutral amino acids indicated that multiple receptor site types with highly overlapping specificities exist to these compounds. For both binary mixtures and multimixtures composed of neutral and basic or neutral and acidic amino acids, the receptor responses were significantly enhanced compared with those mixtures consisting of an equal number of only neutral amino acids. These results demonstrate that receptor sites for the basic and acidic amino acids, respectively, are highly independent of those for the neutral amino acids, and suggest that a mechanism for synergism is the simultaneous activation of relatively independent receptor sites by the components in the mixture. In contrast, there was no evidence for the occurrence of mixture suppression.

scholarly journals Electrophysiological evidence for acidic, basic, and neutral amino acid olfactory receptor sites in the catfish.

1984 ◽  
Vol 84 (3) ◽  
pp. 403-422 ◽  
Author(s):  
J Caprio ◽  
R P Byrd
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Ictalurus Punctatus ◽  
Olfactory Receptor ◽  
Olfactory Receptors ◽  
Receptor Potential ◽  
Side Chains ◽  
Short Side ◽  
Neutral Amino Acids ◽  
Receptor Sites

Electrophysiological experiments indicate that olfactory receptors of the channel catfish, Ictalurus punctatus, contain different receptor sites for the acidic (A), basic (B), and neutral amino acids; further, at least two partially interacting neutral sites exist, one for the hydrophilic neutral amino acids containing short side chains (SCN), and the second for the hydrophobic amino acids containing long side chains (LCN). The extent of cross-adaptation was determined by comparing the electro-olfactogram (EOG) responses to 20 "test" amino acids during continuous bathing of the olfactory mucosa with water only (control) to those during each of the eight "adapting" amino acid regimes. Both the adapting and test amino acids were adjusted in concentrations to provide approximately equal response magnitudes in the unadapted state. Under all eight adapting regimes, the test EOG responses were reduced from those obtained in the unadapted state, but substantial quantitative differences resulted, depending upon the molecular structure of the adapting stimulus. Analyses of the patterns of EOG responses to the test stimuli identified and characterized the respective "transduction processes," a term used to describe membrane events initiated by a particular subset of amino acid stimuli that are intricately linked to the origin of the olfactory receptor potential. Only when the stimulus compounds interact with different transduction processes are the stimuli assumed to bind to different membrane "sites." Four relatively independent L-alpha-amino acid transduction processes (and thus at least four binding sites) identified in this report include: (a) the A process for aspartic and glutamic acids; (b) the B process for arginine and lysine; (c) the SCN process for glycine, alanine, serine, glutamine, and possibly cysteine; (d) the LCN process for methionine, ethionine, valine, norvaline, leucine, norleucine, glutamic acid-gamma-methyl ester, histidine, phenylalanine, and also possibly cysteine. The specificities of these olfactory transduction processes in the catfish are similar to those for the biochemically determined receptor sites for amino acids in other species of fishes and to amino acid transport specificities in tissues of a variety of organisms.

scholarly journals Classes and Narrowing Selectivity of Olfactory Receptor Neurons of Xenopus laevis Tadpoles

2004 ◽  
Vol 123 (2) ◽  
pp. 99-107 ◽  
Author(s):  
Ivan Manzini ◽  
Detlev Schild
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Xenopus Laevis ◽  
Olfactory Receptor ◽  
Developmental Stages ◽  
Olfactory Receptors ◽  
Response Spectra ◽  
Olfactory Receptor Neurons ◽  
Receptor Neurons ◽  
Response Profiles

In olfactory receptor neurons (ORNs) of aquatic animals amino acids have been shown to be potent stimuli. Here we report on calcium imaging experiments in slices of the olfactory mucosa of Xenopus laevis tadpoles. We were able to determine the response profiles of 283 ORNs to 19 amino acids, where one profile comprises the responses of one ORN to 19 amino acids. 204 out of the 283 response profiles differed from each other. 36 response spectra occurred more than once, i.e., there were 36 classes of ORNs identically responding to the 19 amino acids. The number of ORNs that formed a class ranged from 2 to 13. Shape and duration of amino acid-elicited [Ca2+]i transients showed a high degree of similarity upon repeated stimulation with the same amino acid. Different amino acids, however, in some cases led to clearly distinguishable calcium responses in individual ORNs. Furthermore, ORNs clearly appeared to gain selectivity over time, i.e., ORNs of later developmental stages responded to less amino acids than ORNs of earlier stages. We discuss the narrowing of ORN selectivity over stages in the context of expression of olfactory receptors.

Facial Taste Responses of the Channel Catfish to Binary Mixtures of Amino Acids

1999 ◽  
Vol 82 (2) ◽  
pp. 564-569 ◽  
Author(s):  
K. Ogawa ◽  
J. Caprio
Keyword(s):  
Amino Acids ◽  
Binary Mixture ◽  
Binary Mixtures ◽  
Ictalurus Punctatus ◽  
Channel Catfish ◽  
Taste Receptor ◽  
Single Fiber ◽  
Receptor Sites ◽  
Group I ◽  
Group Ii

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.

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