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Department of Medical Psychology, University of Munich Medical School, D-80336 Munich, Germany
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ABSTRACT |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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With use of a conditioning paradigm, the ability of four squirrel monkeys to distinguish n-valeric acid from n-forms and isoforms of other carboxylic acids (acetic acid to octanoic acid) was investigated. All four animals were clearly able to discriminate between all odor pairs tested and showed a significant negative correlation between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length of the carboxylic acids. Branching of the carbon chain was also found to affect odorant quality because all animals performed better in discriminating n-valeric acid from isoforms of other carboxylic acids compared with the corresponding n-forms of these substances. With use of a triple forced-choice procedure, 10 human subjects were tested on the same tasks in parallel and showed a very similar pattern of discrimination performance compared with the squirrel monkeys. Thus the results of this study provide evidence of well-developed olfactory discrimination ability in squirrel monkeys for carboxylic acids and support the assumption that human and nonhuman primates may share common principles of odor quality perception.
olfaction; odor discrimination; nonhuman primates
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INTRODUCTION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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MANY MAMMALIAN SPECIES are capable of recognizing and discriminating among thousands of odors with high sensitivity and specificity. The neural mechanisms underlying this amazing performance are still poorly understood. There is common agreement, however, that odor discrimination begins with differential interaction of odor molecules with different types of olfactory receptors, analogous to the interactions between antigens and antibodies in the immune system, or between neurotransmitters and their receptors in the nervous system (13). To understand how the olfactory system actually achieves odor discrimination, it is therefore clearly important to establish which properties of an odor molecule are functional in determining the degree of interaction with a given receptor and, concomitantly, in determining its perceived odor quality. Furthermore, the assessment of odor structure-activity relationships is also of practical interest to allow prediction of the odor quality of a molecule or of the perceived similiarity between odor molecules (26).
Several studies reported molecular features like carbon chain length or steric conformation to be correlated with perceptibility in terms of detection thresholds when using homologous series of substances as stimuli both in humans (3-6, 29) and in nonhuman mammals (17, 24). Only a few studies, on the other hand, have so far systematically investigated whether such features may also be connected in a regular way with odor quality and thus with perceived similarity between members of a given class of chemicals (12, 19, 35).
One useful means of assessing possible correlations between odor quality and molecular properties is to test the discrimination ability for structurally related odorants that only differ from each other in one feature such as, for example, the number of carbon atoms or the position of a functional group. Furthermore, this method is also applicable to nonhuman species, and a comparative approach to this topic seems particularly reasonable, considering recent findings in the molecular biology of olfaction. A large multigene family coding for putative odor receptors has been identified, and these genes can be grouped into subfamilies on the basis of nucleotide sequence similarity (2). Thus members of a subfamily encode receptors that are highly related in amino acid sequence and therefore are hypothesized to recognize structurally related ligands (25). Furthermore, in situ hybridization experiments using molecular probes for various odorant receptor subtypes suggest that closely related species might have a larger proportion of odor receptors in common compared with phylogenetically more distant species (16, 33).
Because of their close phylogenetic relationship to humans, nonhuman primates may represent a particularly interesting taxon to investigate with regard to similarities and differences in odor quality perception between species. In previous studies, we showed that squirrel monkeys (Saimiri sciureus) can be readily trained to attend to and discriminate between odor stimuli. Using a task based on the discrimination of simultaneously presented odorants (14), reliable measurements of this species' olfactory performance in response to both artificial (18, 20) and natural odors (22) have been obtained, and striking similarities in discrimination ability between Saimiri and humans for artificial odor mixtures (21) and aliphatic esters (19) have been found.
The purpose of the present study is to extend these findings in a first attempt to systematically compare the discrimination ability of human and nonhuman primates for structurally related odorants. We have chosen carboxylic acids, a group of odorants that is made up of important constituents of skin-borne body odors and vaginal secretions in both human (15) and nonhuman primates (10) and thus is presumably of biological significance for both species. Furthermore, we selected stimuli that differ either in length or in branching of the carbon chain, thus making it possible to assess the impact of each for determining the odor quality of a substance.
Thus the aims of the study are threefold: 1) to provide first data on the olfactory discrimination ability of squirrel monkeys for carboxylic acids, 2) to assess whether a correlation between discrimination ability and structural similarity of the odorants under investigation exists, and, 3) by testing a group of human subjects in parallel, to assess whether human and nonhuman primates may share common principles of odor quality perception.
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MATERIALS AND METHODS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Animals. Testing was carried out using two adult female and two adult male squirrel monkeys (Saimiri sciureus) maintained as part of an established breeding colony. All animals had served as subjects in previous olfactory experiments and were completely familiar with the basic test procedure (14, 18-21). The colony was housed in a double enclosure made up of a 23-m3 home cage joined to a 7-m3 test cage by two tunnels that could be closed by sliding doors to allow the temporary separation of animals for individual testing. Animals were provided with marmoset pellets (Ssniff, Soest, Germany), fresh fruit, vegetables, and water ad libitum.
The experiments reported here comply with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health Publication no. 86-23, revised 1985) and also with current German laws.Behavioral test.
In a task designed to simulate olfactory-guided foraging, opaque 1.5-ml
Eppendorf flip-top reagent cups were equipped with absorbent paper
strips (35 × 7 mm; Sugi, Kettenbach, Germany) impregnated with 10 µl of an odorant signaling either that they contained a peanut food
reward (S+) or that they did not (S
). The odor strips were
attached to the vials by cutting a slit in each strip and slipping it
over the flip-up lid which was connected to the vial by a narrow band.
Eighteen such cups, nine positive and nine negative, were inserted in
pseudorandom order in holes along the horizontal bars of a climbing
frame in such a way that some effort was required for the animals to
remove them. The frame was mounted to one of the enclosure walls and
consisted of a 2.5-m vertical pole (40 mm diameter) fitted
with seven cross-bars (20 mm diameter) 30 cm apart, the middle three of
which extended 50 cm to either side and were equipped with conically
bored holes to hold the cups (14).
(Table 1). To prevent
serial order or training effects from confounding the results, the
tasks were not presented according to increasing carbon chain length
(cf. Table 1) but according to increasing structural similarity and
thus presumed similarity in odor quality between S+ and S. Thus
the order of task presentation was
n-valeric acid versus odor
number 7, 1, 6, 2, 10, 8, 5, 3, and
9.
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Human subjects. Ten healthy, unpaid volunteers (7 females and 3 males) 23-36 yr of age participated in the study. All were nonsmokers, and none had any history of olfactory dysfunction. All subjects had previously served in olfactory tests and were familiar with the basic test procedure. They were informed as to the aim of the experiment and provided written consent. The study was performed in accordance with the Declaration of Helsinki/Hong Kong.
Test procedure. A 40-ml aliquot of each odorant was presented in a 250-ml polyethylene squeeze bottle equipped with a flip-up spout that for testing was fitted with a custom-made Teflon nosepiece. Subjects were instructed as to the manner of sampling and at the start of the first session were allowed time to familiarize themselves with the bottles and the sampling technique. Care was taken that the nosepiece was only a short distance (1-2 cm) from the nasal septum during sampling of an odorant to allow the stimulus to enter both nostrils.
In a forced-choice triangular test procedure, subjects were asked to compare three bottles and identify the one containing the odd stimulus. Additionally, after each decision subjects were asked whether their choice was predominantly based on perceived differences in odor quality or on perceived differences in odor intensity. Each bottle could be sampled two times, with an interstimulus interval of at least 10 s. Sampling duration was restricted to 1 s per presentation to minimize adaptation effects. The sequence of presenting the stimulus pairs was systematically varied between sessions and individual subjects while taking care to avoid successive presentations of the same combinations and while systematically varying the order in which the stimuli were sampled. The presentation of n-valeric acid as odd or even stimulus was balanced within and between sessions. Approximately 30 s were allowed between trials, and no feedback regarding the correctness of the subjects' choice was given. Ten different stimulus pairs, the same ones as for the squirrel monkeys, were presented two times per session so as to give a total of 20 judgments. Testing was repeated in four more sessions, each 1-3 days apart, enabling 10 judgments per stimulus pair and panelist to be collected.Odorants. A set of 11 odorants was used (Table 1). All substances had a nominal purity of at least 99%. They were diluted using diethyl phthalate (Merck) as the solvent. In an attempt to ensure that the odorants were of approximately equal strength when presented on the absorbent paper strips, intensity matching was performed by a panel using freshly prepared strips impregnated with 10 µl of a 8.7 g/l solution of isoamyl acetate as the standard and adopting a standardized psychophysical procedure (1). This was chosen 1) because this odorant and concentration had been successfully used in previous studies (17, 18) and 2) to provide odor concentrations that could be reliably detected by the animals but weak enough to prevent contamination of the test cage and to force the animals to sniff closely.
Likewise, in an attempt to ensure that the odorants were of approximately equal strength when presented in squeeze bottles, intensity matching was performed by a panel using a 8.7 g/l solution of isoamyl acetate as the standard and adopting a standardized psychophysical procedure (1). Because the mode of presentation of odorants differed between squirrel monkeys (absorbent paper strips, i.e., an open system allowing odorants to diffuse freely) and humans (squeeze bottles, i.e., a closed system allowing odorants to build an equilibrium in the headspace), the concentrations used for the two species differed for some of the odorants (cf. Table 1).Data analysis. In assessing performance of the squirrel monkeys, only cups inspected by the animals were scored. For each individual, the percentage of correct choices from the best two sessions, that is, from 10 1-min trials comprising a total of at least 60 decisions, was calculated. Correct choices consisted of animals both correctly rejecting negative cups by failing to open or remove them and in identifying positive cups by removing and opening them to obtain the food reward. Conversely, errors consisted in animals opening or removing negative cups or failing to remove and open positive cups.
Significance levels for both squirrel monkeys and human subjects were determined by calculating binomial z scores corrected for continuity (31) from the number of correct and false responses for each individual and condition. Comparisons across tasks were made using Friedman's two-way ANOVA. When ANOVA detected differences between tasks, this was then followed by pairwise Wilcoxon's signed-rank tests for related samples to evaluate which tasks were responsible. Correlations between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length were evaluated using Spearman's rank correlation coefficient and tested for significance by computing t values (31). All tests were two-tailed, and the alpha level was set at 0.05. All data are reported as means ± SD.| |
RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Squirrel monkeys. Figure 1 summarizes the mean performance of the squirrel monkeys in discriminating n-valeric acid from other carboxylic acids. All four animals performed significantly above chance level in all tasks, usually scoring around 80% correct choices, and thus were clearly able to discriminate between all odor pairs presented (binomial test, P < 0.001 for all tasks and individuals). Interindividual variability was low and generally <20% between the highest- and lowest-scoring animal (cf. SDs in Fig. 1). In the majority of cases, their scores were in the range of the easy-to-solve control task (n-valeric acid vs. anethole). However, ANOVA detected significant differences in the animals' performance between tasks (Friedman's test, P < 0.001), and subsequent pairwise tests revealed that three of the substances (n-butyric acid, n-hexanoic acid, and isovaleric acid) were significantly more difficult to discriminate from n-valeric acid compared with the control and most of the other tasks (Wilcoxon's test, P < 0.05).
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Human subjects. Figure 3 summarizes the mean performance of human subjects in discriminating n-valeric acid from other carboxylic acids. As a group, the human subjects performed significantly above chance level in all tasks and thus were clearly able to discriminate between all odor pairs presented (binomial test, P < 0.001 for all tasks), although marked interindividual differences in performance were apparent (cf. SDs in Fig. 3). In only three out of nine tasks were mean scores in the range of the easy-to-solve control task (n-valeric acid vs. anethole). ANOVA detected significant differences in the human subjects' performance between tasks (Friedman's test, P < 0.001), and subsequent pairwise tests revealed that five of the substances (n-butyric acid, n-hexanoic acid, isobutyric acid, isovaleric acid, and isohexanoic acid) were significantly more difficult to discriminate from n-valeric acid compared with the control and the other tasks (Wilcoxon's test, P < 0.05). Accordingly, 5 (isovaleric acid), 4 (n-butyric acid), 2 (isobutyric acid) and 1 (n-hexanoic acid and isohexanoic acid) out of 10 individuals failed to significantly discriminate the respective substances from n-valeric acid (binomial test, P > 0.05). Figure 4 shows that the differences in performance of the human subjects among the six tasks that involved the discrimination of n-carboxylic acids followed the same systematic pattern as in the squirrel monkeys: again, odor pairs that only differed by one carbon atom were significantly more difficult to discriminate than odor pairs that differed by two or three carbon atoms (Wilcoxon's test, P < 0.01), and odor pairs differing by two carbon atoms were significantly more difficult to distinguish compared with odor pairs that differed by three carbon atoms (Wilcoxon's test, P < 0.01). Thus a significant negative correlation between discrimination performance of the human subjects and structural similarity of odorants in terms of differences in carbon chain length of the n-carboxylic acids was found (Spearman's rank correlation coefficient, P < 0.01).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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The results of this study demonstrate that 1) squirrel monkeys possess a well-developed olfactory discrimination ability for carboxylic acids, 2) a significant negative correlation exists between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length, 3) differences in steric conformation also affected stimulus quality and thus discriminability of the odorants, and 4) human subjects tested on the same tasks in parallel showed a very similar pattern of discrimination performance compared with the squirrel monkeys.
Although only four animals were tested, the results appear robust, because interindividual variability of scores was low and the general pattern of performance across tasks was almost identical between individual monkeys (Spearman's rank correlation coefficient, P < 0.01). Furthermore, two of the experimental conditions (n-valeric acid vs. isovaleric acid and n-valeric acid vs. isohexanoic acid) were retested after 6 wk and generally yielded very similar scores compared with their initial presentation (Fig. 5), thus supporting the assumption that the results are not flawed by serial order or training effects but truly reflect differences in discrimination performance between tasks.
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Given the presumed biological significance of carboxylic acids as qualitatively and quantitatively predominant constituents of primate skin-borne body odors (9) and vaginal secretions (11, 23), the finding of a well-developed olfactory discrimination ability in a nonhuman primate species for this group of substances may not seem surprising. However, it should not be forgotten that in the real world odors are usually perceived in a given context together with numerous nonolfactory cues that might help an animal to associate the odor with an odor source or a certain meaning. In our rather artificial experimental setup, however, there were no such contextual cues, and therefore we think that the tasks used were not at all trivial, an appraisal that is supported by the performance of the human subjects tested in parallel. Furthermore, the good performance of Saimiri sciureus in the present study is in accordance with earlier reports of a highly developed discrimination ability in this species for artificial odor mixtures (21), conspecific urine odors (22), and aliphatic esters (19) and thus lends additional support to the accumulating evidence that olfaction may play a significant role in the regulation of primate behavior (10).
It is well established that the vast majority of odorants have, at high concentrations, some trigeminal-stimulating properties (7). This raises the possibility that the discrimination performance of both humans and squirrel monkeys in the present study may not have been achieved by the olfactory system alone but may have involved the trigeminal system as well. A recent psychophysical study (6), however, has shown nasal pungency thresholds (mediated by the trigeminal nerve) of human subjects for the same carboxylic acids as used here to be at least three orders of magnitude higher compared with odor thresholds (mediated by the olfactory nerve). Thus, at least for the human subjects tested here, the possibility of trigeminal involvement in the discrimination of odorants can be excluded. Although corresponding data on nasal trigeminal sensitivity for carboxylic acids in the squirrel monkey are missing, there is no reason to believe that Saimiri differs fundamentally from humans or other vertebrate species in this respect. Both behavioral and electrophysiological studies using the rat, the salamander (32), and the pigeon (34) suggest the nasal trigeminal system to be considerably less sensitive compared with the olfactory system in general and to be incapable of discriminating between intensity-matched odorants.
Although the possibility that differences in perceived odor intensity
might have contributed to the good discrimination performance in both
species cannot be ruled out completely, this seems quite unlikely
because the reliability of our intensity-matching procedure was
confirmed by the fact that, during the critical discrimination tasks,
>90% of the subjects' decisions were reported to be based on
perceived differences in odor quality rather than odor intensity (cf.
Test procedure). Furthermore, we
could show in an earlier study (21) that the discrimination scores of
our squirrel monkeys remained quite stable even when the concentration
of the S was one order of magnitude higher or lower than the
concentration matched to the S+. Therefore, we believe the
discrimination scores of both species reflect the ability of their
olfactory systems to distinguish between odor qualities.
To the best of our knowledge, no other study so far has assessed the olfactory discrimination abilities of other, nonprimate species for carboxylic acids. The few studies, however, that so far have systematically investigated correlations between carbon chain length and odor quality in other homologous series of substances are in line with the results of the present study because they too suggest the existence of such regular connections within a given class of chemicals. In tests of human subjects, two psychophysical studies (8, 27) have reported perceptual similarity between members of a homologous series of aliphatic alcohols to be positively correlated with similarity in carbon chain length. Using the same methodology as in the present study, we found a significant negative correlation between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length of aliphatic esters in squirrel monkeys and humans (19). The results of both the present study and our earlier study also correspond with electrophysiological findings that showed the tuning specificities of mouse olfactory receptor neurons to correlate with carbon chain length of aliphatic esters and carboxylic acids (30). Thus both the behavioral and the electrophysiological findings suggest carbon chain length of aliphatic odorants to be one of presumably several determinants of the interaction between stimulus molecule and receptor.
With regard to steric conformation of odorants, the second molecular feature investigated here, other studies found discrimination ability usually to be odor-pair specific, ranging from easily distinguishable odor pairs to indiscriminable ones, with no recognizable correlation between odor quality and this structural property of the stimulus (12, 28, 36).
We found n- and isovaleric acid to be discriminable for both squirrel monkeys and humans, but the comparatively poor performance of both species in this task suggests that these two substances are qualitatively similar despite different steric conformation. It is interesting to note, however, that all four squirrel monkeys scored slightly better in the discrimination between n-valeric acid and isobutyric acid compared with the discrimination between n-valeric acid and n-butyric acid (cf. Fig. 1). Similarly, all four animals had more difficulties in discriminating between n-valeric acid and n-hexanoic acid than between n-valeric acid and isohexanoic acid, and exactly the same pattern was found for the mean performance of the human subjects (cf. Fig. 3). This suggests that differences in steric conformation in terms of presence or absence of branching of the carbon chain may also affect odor quality and thus discriminability of carboxylic acids in both human and nonhuman primates.
Although the different methodologies used with humans and squirrel monkeys do not allow valid comparisons of absolute discrimination scores between species, it seems admissible to compare the patterns of discrimination performance across tasks found with each species. In the present study, humans and squirrel monkeys showed apparent similarities in their relative discrimination performance, with both species scoring worst in the tasks n-valeric acid versus n-butyric acid and n-valeric acid versus isovaleric acid and both species scoring best in the tasks n-valeric acid versus acetic acid and n-valeric acid versus n-octanoic acid (cf. Figs. 1 and 3). Furthermore, both species showed a significant negative correlation between discrimination performance and structural similarity of odorants (cf. Figs. 2 and 4). These findings are in accordance with earlier reports that showed squirrel monkeys and humans to correspond in their patterns of discrimination ability for artificial odor mixtures that had been systematically varied in similiarity in terms of the number of components the discriminants shared (21) and in their relative discrimination performance for aliphatic esters (19).
Thus the results of the present study support the assumption that humans and squirrel monkeys may share common principles of odor quality perception. Furthermore, they support the current concept of stimulus molecules having multiple epitopes that may interact independently of each other with complementary sites or ligand binding domains of the molecular receptor protein (36). Given the recent advances in the understanding of the bimolecular process underlying the initial step of olfactory perception (13), it seems worthwhile pursuing our comparative approach to odor quality perception and discrimination using further groups of structurally related substances.
Perspectives
This study provided evidence for striking similarities in the relative discrimination performance of humans and squirrel monkeys for a homologous series of odor substances. These findings lend support to the assumption that closely related species might have a larger proportion of molecular odor receptors in common compared with phylogenetically more distant species (16, 33). However, to further corroborate this hypothesis, it is clearly important to include other, preferably nonvertebrate species into corresponding studies of olfactory discrimination ability using the same stimuli. Additionally, it would be desirable to include an Old World primate species that is even more similar to humans than Saimiri sciureus into such a comparative approach.Furthermore, our findings imply that it would be useful to perform comparative studies on olfactory discrimination ability using other classes of odorant substances. This would allow us to assess whether the conformity in relative performance found between the two primate species in the present study is restricted to the particular set of odor stimuli tested here or whether it may represent a more generalizable phenomenon that holds true for a larger part or even the whole spectrum of odors.
Testing different species with the same sets of homologous series of odorants using reliably comparable psychophysical procedures would also allow us to draw conclusions as to the nature and generality of odor structure-activity relationships across the animal kingdom and thus appears to be a promising tool to further elucidate the molecular mechanisms underlying the perception of odor quality.
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ACKNOWLEDGEMENTS |
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We thank Detlev Ploog for providing us with the animals and much helpful advice and the Deutsche Forschungsgemeinschaft for financial support (La 635/6-1).
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FOOTNOTES |
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Address for reprint requests: M. Laska, Dept. of Medical Psychology, Univ. of Munich Medical School, Goethestr. 31, D-80336 Munich, Germany.
Received 1 December 1997; accepted in final form 27 February 1998.
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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C).
,
female; 
, male.