Fish Smell. Focus on “Odorant Specificity of Single Olfactory Bulb Neurons to Amino Acids in the Channel Catfish”

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.

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Electrophysiological responses of single olfactory bulb neurons to amino acids in the channel catfish, Ictalurus punctatus

Journal of Neurophysiology ◽

10.1152/jn.1995.74.4.1421 ◽

1995 ◽

Vol 74 (4) ◽

pp. 1421-1434 ◽

Cited By ~ 11

Author(s):

J. Kang ◽

J. Caprio

Keyword(s):

Amino Acids ◽

Amino Acid ◽

Olfactory Bulb ◽

Ictalurus Punctatus ◽

Channel Catfish ◽

Action Potentials ◽

Recording Time ◽

Over Time ◽

Olfactory Bulb Neurons

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.

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

Journal of Neurophysiology ◽

10.1152/jn.2001.86.4.1869 ◽

2001 ◽

Vol 86 (4) ◽

pp. 1869-1876 ◽

Cited By ~ 59

Author(s):

Alexander A. Nikonov ◽

John Caprio

Keyword(s):

Amino Acids ◽

Olfactory Bulb ◽

Ictalurus Punctatus ◽

Channel Catfish ◽

Bile Salts ◽

Spatial Organization ◽

Field Potential ◽

Specific Class ◽

Biologically Relevant ◽

Excitatory Responses

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.

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Odorant Specificity of Single Olfactory Bulb Neurons to Amino Acids in the Channel Catfish

Journal of Neurophysiology ◽

10.1152/jn.00023.2004 ◽

2004 ◽

Vol 92 (1) ◽

pp. 123-134 ◽

Cited By ~ 60

Author(s):

Alexander A. Nikonov ◽

John Caprio

Keyword(s):

Amino Acids ◽

Olfactory Bulb ◽

Channel Catfish ◽

Monosodium Glutamate ◽

Side Chains ◽

Low Concentration ◽

Receptor Sites ◽

Group I ◽

Methylene Groups ◽

Guanidinium Group

Odorant specificity to l-α-amino acids was determined for 245 olfactory bulb (OB) neurons recorded from 121 channel catfish. The initial tests included 4 amino acids representing acidic [monosodium glutamate (Glu)], basic [arginine (Arg)], and neutral [possessing short: alanine (Ala) and long: methionine (Met) side chains] amino acids that were previously indicated to bind to independent olfactory receptor sites. Ninety-one (37%) units (Group I) tested at 1, 10, and 100 μM showed high selectivity and were excited by only one of the 4 amino acids. Odorant specificity for the vast majority of Group I units did not change over the 3 s of response time analyzed. A total of 154 OB units (63%) (Group II) were excited by a second amino acid, but only at ≥10× odorant concentration. An additional 69 Group I units were tested with related amino acids and derivatives from 10−9 to 10−5 M to determine their excitatory odorant thresholds and selectivities. Two groups of units originally selective for Met were evident: those most sensitive to neutral amino acids having branched and linear side chains, respectively. OB units originally selective for Ala responded at low concentration to other similar amino acids. Units originally selective for Arg were excited at low concentration by amino acids possessing in their side chains at least 3 methylene groups and a terminal amide or guanidinium group. The specificities of the OB units determined electrophysiologically are sufficient to account for many of the previous results of behavioral discrimination of amino acids in this and related species.

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