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Department of Zoology and Physiology, Louisiana State University, Baton Rouge, Louisiana 70803-1725
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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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).
Physiological investigations of vertebrate olfaction have generally studied how the olfactory system responds to single odorants. Under natural circumstances, however, odorants are primarily complex mixtures of chemicals. A major question critical for a better understanding of olfaction is whether olfactory receptor neurons respond to odorant mixtures differently, due to mixture interactions, than to individual odorants. The most frequently cited mixture interactions for chemosensory responses are mixture suppression and synergism (Bartoshuk and Gent 1985 Animal maintenance, preparation, stimulus delivery, electrophysiological methods, and data acquisition are identical to those published previously (Kang and Caprio 1995b Chemical stimuli
Individual stimuli were four L-amino acids, alanine (Ala, a neutral amino acid with a short side-chain), arginine (Arg, a basic amino acid), glutamic acid (Glu, an acidic amino acid), and methionine (Met, a neutral amino acid with long side chains; Sigma grade; Sigma Chemical, St. Louis, MO). These amino acids were previously indicated from cross-adaptation (Caprio and Byrd 1984 Data analysis
Responses of single olfactory receptor neurons to binary mixtures and to their components were classified as excitatory (E), suppressive (S), or null (N) based on the interrupted time-series analysis (Crosbie 1993 Spontaneous activity for 54 olfactory receptor neurons from 23 channel catfish (24-74 g) was 28 ± 18 (mean ± SD; range, 1-95) action potentials/5 s. The receptor neurons were tested with 128 binary mixtures (excluding repeated trials on the same unit) consisting of the 6 possible pairings of the 4 amino acids. Each binary mixture evoked different types of responses across the different olfactory receptor neurons tested (Figs. 1 and 2). The evoked responses were not associated with specific stimulus mixtures (
Component-similar binary mixtures
Fifty-nine tests were performed with binary mixtures whose component responses were similarly classified as both excitatory (E), both suppressive (S), or both null (N), respectively. For these 59 component-similar mixtures, 80% resulted in the same response types as their components.
CATEGORY I (E+E MIXTURES).
Only two E+E binary mixtures were tested and both evoked excitatory responses. The mean percent response change to the two E+E mixtures was not significantly different from that to the components.
CATEGORY II (S+S MIXTURES).
Eighty-six percent (n = 19) of the 22 S+S binary mixtures tested resulted in suppression, whereas 14% (n = 3) failed to elicit responses significantly different from spontaneous activity, i.e., "null" (N) activity (Figs. 3A and 4Aa). The mean percent response change to the S+S mixtures that evoked suppressive responses was not significantly different from that to the components (Fig. 3A). Also, no significant difference in the spontaneous rate of action potentials for 5 s of prestimulation was observed for units that responded to the S+S mixtures with suppression and null activity, respectively (Table 1).
CATEGORY III (N+N MIXTURES).
Seventy-four percent (n = 26) of the 35 N+N binary mixtures tested resulted in null activity, 12% (n = 4) evoked excitatory responses, and 14% (n = 5) elicited some suppression of spontaneous activity (Figs. 3B and 4Aa). The mean percent response change to the N+N mixtures that evoked null responses was not significantly different from that to their components (Fig. 3B). Also no significant difference in the spontaneous rate of action potentials for 5 s of prestimulation was observed for units that responded to the N+N mixtures with null, excitatory, and suppressive activity, respectively (Table 1).
Component-different binary mixtures
Sixty-nine tests were performed with binary mixtures whose component amino acids elicited different types of responses (E+N, S+N, and E+S). Overall, only five (7%) mixtures elicited a response type that was not observed in the response to one of the component amino acids.
CATEGORY IV (E+N MIXTURES).
Thirty-eight percent (n = 8) of 21 E+N binary mixtures tested evoked excitatory responses, whereas 62% (n = 13) resulted in null activity (Figs. 3C and 4Ab). The mean percent response change to the E+N mixtures that evoked excitatory responses and those E+N mixtures that resulted in null activity was not significantly different from that to their E and N components, respectively (Fig. 3C). The spontaneous rate of action potentials for 5 s of prestimulation was, however, significantly greater for the units that responded to E+N mixtures with null activity than for those that were excited (Table 1).
CATEGORY V (S+N MIXTURES).
Thirty-two percent (n = 12) of 37 S+N binary mixtures tested elicited suppressive responses, whereas 68% (n = 25) resulted in null activity (Figs. 3D and 4Ab). The mean percent response change to the S+N mixtures that resulted in suppressive responses and those S+N mixtures that resulted in null activity was not significantly different from that to the S and N components, respectively (Fig. 3D). The spontaneous rate of action potentials for 5 s of prestimulation for olfactory receptor neurons that were suppressed by the S+N mixtures was significantly greater than for those units that responded with null activity (Table 1).
CATEGORY VI (E+S MIXTURES).
Twenty-seven percent (n = 3) of 11 E+S binary mixtures tested evoked excitatory responses, 18% (n = 2) elicited suppressive responses, and 55% (n = 6) resulted in null activity (Figs. 3E and 4Ab). The mean percent response change to both the E+S mixtures that resulted in excitatory responses and to the E+S mixtures that resulted in suppressive responses was not significantly different from that to the E and S components, respectively (Fig. 3E). The spontaneous rate of action potentials for 5 s of prestimulation was not significantly different among the olfactory receptor neurons that responded to the E+S mixtures with either null, excitatory, or suppressive responses (Table 1).
Component-similar mixtures
The present results demonstrated that 80% (47 of 59) of the responses of the single olfactory receptor neurons recorded to component-similar (i.e., E+E, S+S, and N+N) binary mixtures were similar to the responses to their components (Fig. 4Aa), which suggest that profound mixture interactions for component-similar mixtures are rare for channel catfish olfactory receptor neurons. These results are equivalent to the previous results that 82% (108 of 131) of the responses of single olfactory bulb neurons in the channel catfish to component-similar binary mixtures were similar to the responses to their components (Fig. 4Ba) (Kang and Caprio 1995a Component-different mixtures
Responses of single olfactory receptor neurons to E+N and S+N mixtures were similar to the response to one of the components (Fig. 4Ab). For 38% of the tests of E+N mixtures and 32% of the tests of S+N mixtures, excitatory and suppressive responses, respectively, were evoked from single olfactory receptor neurons. Thus, for 62% of the tests of the E+N mixtures and 68% of the tests of the S+N mixtures, the N components effectively masked the effectiveness of the E and S components, respectively. Studies of brain interneurons of the spiny lobster (Ache 1989 Relation to previous studies of olfactory receptor responses to stimulus mixtures in the channel catfish
Previously published results of responses of olfactory receptor neurons of channel catfish to stimulus mixtures were obtained from populations of receptor cells (Caprio et al. 1989 Component qualities in binary mixtures
In the present study, 86% of the responses of olfactory receptor neurons to the tested binary mixtures were classified similarly to at least one of the stimulus components. This percentage for responses of olfactory receptor neurons was matched (i.e., 89%) by the responses of single olfactory bulb neurons in the same species to similar binary mixtures (Kang and Caprio 1995a
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Carr and Derby 1986a,b; Derby and Ache 1984; Johnson et al. 1989). Mixture suppression is inferred if the measured response to a mixture is significantly less than the predicted response, whereas synergism is indicated if the measured response is significantly greater than predicted. Many of the previous investigations of olfactory responses to stimulus mixtures utilized crustaceans as experimental models (Atema et al. 1989; Borroni et al. 1986; Carr and Derby 1986a,b; Derby and Ache 1984; Derby et al. 1985, 1991a,b; Gleeson and Ache 1985; Johnson et al. 1985, 1989; Zimmer-Faust et al. 1984). Many of these earlier studies indicated that because of mixture interactions the response to a mixture was difficult to predict, even when the responses to the individual components were known. This general result implied that possibly a new coding principle, different from that utilized for single odorants, was employed when olfactory receptor neurons simultaneously detect multiple odorants. A more recent investigation indicated, however, that population responses of lobster antennule neurons to binary mixtures are generally predictable by taking into account not only the odorant responses to the individual components of the mixture, but also competitive and noncompetitive effects of stimulus-receptor binding (Daniel et al. 1996).
). No comparable data for responses of single olfactory receptor neurons to odorant mixtures was, however, previously available.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). The electroolfactogram (EOG) was used as an indicator of both the viability of the preparation and the time of response onset, because the latter for an individual receptor neuron can sometimes be difficult to detect.
) and receptor binding (Bruch and Rulli 1988) studies to bind to relatively independent olfactory receptor sites in the channel catfish. With the exception of 10
3 M Glu, the amino acids were tested individually at 104 M, stimulus concentrations adjusted to the nearest whole log unit of concentration that elicited similar EOG magnitudes (Kang and Caprio 1991). Stock solutions (102 M) were prepared weekly with charcoal-filtered artesian tap water (pH ~8.5) and stored at 4°C. During the experiments, stimulus solutions were prepared by diluting the stock solutions with charcoal-filtered artesian tap water to the desired concentrations. Binary mixtures included all pairings of the four tested amino acids. The mixtures were formed by mixing equal aliquots of two amino acid solutions at double the concentrations used for testing the individual components. Thus, because of the 50% dilution of each component by the other component, the concentrations of the individual components in the binary mixtures were identical to the concentrations of the components tested individually.
; Hudson 1977). The analysis was conducted on the number of action potentials within successive 200-ms time bins for 5 s before and during odor stimulation.
where PRE and POST are the number of action potentials occurring during 5-s prestimulation and 5-s stimulation periods, respectively. The mean percent response changes between specific mixtures and components were analyzed by paired t-tests (a = 0.05).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
2 = 10.2,P > 0.5, df = 10). However, the responses of single olfactory receptor neurons to binary mixtures were similar to the responses to at least one of the components (Figs. 1 and 2), and the response types to the mixtures were highly associated with the responses elicited by the component stimuli (2 = 73.8, P < 0.001, df = 10).
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FIG. 1.
Examples of responses of single olfactory receptor neurons to binary mixtures and to their components. A: S+S mixtures. Duplicate suppressive responses to L-arginine (Arg; a) and to L-glutamic acid (Glu; b) and to the binary mixture (c). B: E+N mixtures. Duplicate null responses to Arg (a), duplicate excitatory responses to Glu (b), and duplicate excitatory responses to the binary mixtures (c). The concentrations of Arg and Glu in the binary mixtures (c) were equal to those tested individually in a and b, respectively. Dotted lines indicate the onset of the neural responses based on the onset of the electroolfactogram (EOG; not shown).
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FIG. 2.
Summary of responses of single olfactory receptor neurons to binary mixtures of amino acids and to their individual components. Abscissa indicates neuron number. PRE and POST indicate the number of action potentials occurring during the 5-s prestimulation and 5-s stimulation periods, respectively. The percent response changes that are >100% are standardized to 100%. n = total number of receptor neurons tested with each respective mixture and components.
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FIG. 3.
Summary of responses of olfactory receptor neurons to binary mixtures and to their individual components. Data in this figure are the same as those presented in Fig. 2, but are organized according to the response types evoked by the components, i.e., excitatory (E) and suppressive (S) responses and null (N) activity. All response types were classified according to the interrupted time-series analysis (Crosbie 1993 ; Hudson 1977). Abscissa indicates neuron number. The n adjacent to mixture categories (A-E) indicates the total number of neurons tested with each respective mixture and its components. The number (n) of neurons that responded with either E, S, or N activity to the different mixture types are included within the respective section of each summary box.
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FIG. 4.
Comparison of responses of olfactory receptor (A) and bulb (B) neurons to binary mixtures of amino acids. a: responses to component-similar mixtures. b: responses to component-different mixtures. B is modified from Fig. 4 in Kang and Caprio (1995a) .
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TABLE 1.
Analyses of the mean number of action potentials occurring in 5 s before stimulation
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
).
; Ache et al. 1988; Derby et al. 1991a; Gleeson and Ache 1985; McClintock and Ache 1989; Michel et al. 1991) and/or noncompetitive (Bell et al. 1987; Laing and Glemarec 1992) inhibitory interactions between the stimuli at the receptor sites.
) and mixture (Caprio et al. 1989; Kang and Caprio 1991) studies were consistent in indicating that the component amino acids tested in the present study bound to relatively independent olfactory receptor sites. The combination of two amino acids that interact with different receptor sites, but having some overlapping specificities (Kang and Caprio 1991; Imamura et al. 1992), might result in effectively increasing the stimulus concentration of one of the components producing a suprathreshold stimulus resulting in either E or S type activity. Finally, no significant differences in the spontaneous activity of the different olfactory receptor units occurred that might have accounted for any of the above listed unpredictable responses to the component-similar binary mixtures (Table 1).
; Derby and Ache 1984; Derby et al. 1985) and deuocerebral neurons of the potato beetle (De Jong 1988) indicated that compounds that individually did not evoke excitatory responses from the respective neurons suppressed the efficiency of excitatory components when combined to form mixtures. Thus a "null" component can mask either an excitatory or a suppressive component. The term "mixture masking" used in both the present study of olfactory receptor neuron responses and in a previous report on responses of single olfactory bulb neurons to binary mixtures (Kang and Caprio 1995a) has a broader meaning than the term "mixture suppression" used in other previous studies (Ache 1989; Boeckh 1967; Derby and Ache 1984; Derby et al. 1985). In mixture suppression, one component in a mixture only suppresses the neuron's excitatory response to the other component, but in mixture masking, a component reduces or conceals the neuron's excitatory or suppressive response to the other component. The masking of the E response by the N component might be considered an example of mixture suppression, whereas the masking of the S component by the N component might be considered a case of mixture enhancement. The mixture masking effect observed at the level of single olfactory receptor neurons is likely to be the result of peripheral mechanisms of competitive and/or noncompetitive inhibition. The previous suggestion that the mixture masking effect observed at the single olfactory bulb cell level (Fig. 4Bb) might be due partially to neural mechanisms within the CNS (Kang and Caprio 1995a) is now doubtful because of the even greater percentage of mixture-masking effects presently observed at the sensory cell level. The reduction of this effect at the olfactory bulb level could be due to the convergence of olfactory receptor neurons that responded to both E+N and S+N binary mixtures with statistically nonsignificant elevation and reduction, respectively, in numbers of action potentials observed at the sensory cell level. With convergence of these respective fibers to their targets in the olfactory bulb, responses of mitral cells that were significantly enhanced and suppressed, respectively, could have occurred.
; Kang and Caprio 1991). EOG and integrated neural responses from populations of olfactory receptor neurons to amino acid odorants were always excitatory, and the magnitude of the excitatory responses to the respective mixtures were predictable. This predictability was based on knowledge of the relative independence of the receptors for the component stimuli obtained from electrophysiological cross-adaptation (Caprio and Byrd 1984) and receptor binding (Bruch and Rulli 1988) experiments. Although the population response to amino acids was always excitatory, 66% of the responses of single olfactory receptor neurons in channel catfish to odorants, including amino acids, were suppressive (Kang and Caprio 1995b). Because averaged spontaneous frequency of single olfactory receptor neurons ranged from <1 to 19 action potentials/second, with a mean frequency of 5.6 action potentials/second, excitatory responses of neurons within a population of olfactory receptor neurons could easily conceal the smaller response (the reduction from spontaneous activity) occurring in other neurons of the population. Also, the magnitude of the odorant-induced dc change (EOG) in the water above the olfactory organ reflects the averaged result of all depolarizations and hyperpolarizations of the responding population of olfactory receptor neurons; however, upon strong depolarization, the membrane potentials of single sensory neurons could shift from resting potential by >100 mV, which would dwarf any odor-induced hyperpolarizations of other receptor neurons. Because individual sensory neurons can be either excited, suppressed or be nonresponsive to an odorant, the methodology used in the previous studies of only averaged excitatory responses was not applicable for all tests of components and stimulus mixtures in the present study. However, in the two cases of E+E mixtures, the components (Arg and Glu) were both excitatory, were tested at approximately equipotent concentrations, and were indicated to bind to relatively independent receptor sites (i.e., "across-group" mixtures) (Caprio et al. 1989). For these mixtures, the calculated mixture discrimination index [MDI; response (number of action potentials elicited during the initial 5 s of response minus that occurring during 5 s of prestimulus activity) to the mixture divided by the average of the responses to the 2 approximately equipotent components that were mixed in equal proportions to form the mixture)] (Caprio et al. 1989; Hyman and Frank 1980), for the two units was 1.24 and 3.38, respectively. The former was less than and the latter was greater than the average MDI calculated for binary across-group mixtures (comprised of components that do not cross-adapt) based on both EOG and integrated neural activity. In both cases, however, the MDI for these across-group mixtures was greater than the average MDI for "within-group" mixtures (comprised of components that are cross-adaptive) based on the population response (Caprio et al. 1989). The independent component index (Caprio et al. 1989; Hyman and Frank 1980) could not be calculated in the present experiments because the necessary stimulus concentrations for its determination were not tested.
). Although mixture interactions were documented in the present and previous (Kang and Caprio 1995a) reports, there is sufficient evidence to suggest that the qualities of components within simple odorant mixtures are not often lost, which is similar to that previously reported in honeybees (Getz and Smith 1987, 1990; Smith and Getz 1994), lobster (Derby et al. 1996), and humans (Laing and Willcox 1983). It is, therefore, highly unlikely that a coding principle, different from that utilized for single odorants, is employed by the olfactory system when olfactory receptor neurons simultaneously detect rather simple odorant mixtures. Whether the binary mixtures employed in the present report are perceived by the channel catfish through olfaction as (or similar to) the component quality or as a novel odorant different from that to either components may be answered through the development of specific whole animal behavioral bioassays, because it is known that olfaction and not taste in this species facilitates the conditioned discrimination of amino acids (Valentincic et al. 1994).
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ACKNOWLEDGEMENTS |
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We thank Dr. R. Voigt for the basic-language programs that aided our computer analysis of the data, two anonymous referees for constructive criticisms, and R. Bouchard for photographic assistance.
This work was supported by grants from the Office of Naval Research (N00014-90-J-1583) and the National Science Foundation (IBN-9221891).
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FOOTNOTES |
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Present address of J. Kang: Monell Chemical Senses Center, 3500 Market Street, Philadelphia, PA 19104.
Address reprint requests to J. Caprio.
Received 26 April 1996; accepted in final form 9 September 1996.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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