Potentiation and overshadowing in odor-aversion learning: Role of method of odor presentation, the distal-proximal cue distinction, and the conditionability of odor

LEARNING

AND

MOTIVATION

17, 115-138 (1986)

Potentiation and Overshadowing in Odor-Aversion Learning: Role of Method of Odor Presentation, the Distal-Proximal Cue Distinction, and the Conditionabilityof Odor MARK

E. BOUTON, DAVID L. JONES, SHEILA A. MCPHILLIPS, AND DALE

SWARTZENTRUBER

Four experiments with rat subjects examined interactions between odors and tastes in com~und aversion conditioning. In Experiments I and 2, a saccharin taste potentiated the conditioning of an almond odorant presented on a cup near the location of the drinking spout, but overshadowed the same odorant when it was mixed in drinking water. This difference depended on the type of odor administered during con~tioning rather than testing (Expe~ment 2). Experiments 3 and 4 examined implications of two other differences between the cup and drink odors: (1) while the cup odor was a distal cue that suppressed approach to the spout, the drink odor was primarily a proximal cue that suppressed consumption, and (2) the cup odor was less conditionable than the drink odor when the stimuli were conditioned aione. In Experiment 3, unlike the proximal saccharin taste, the proximal drink odor failed to potentiate the conditioning of a different distal odor. In Experiment 4, substantial dilution of the proximal drink’s concentration resulted in both weaker conditioning of the stimuIus alone, and potentiation of its conditioning by saccharin. The results suggest that the difference in the conditionability of the cup and drink odors, and not their status as distal and proximal cues, may be critical in the production of potentiation. Weakly conditionable target stimuli are uniquely potentiated by saccharin. % 1986Academic press, Inc.

Most theories of conditioning assume that conditioned stimuli (CSs) will compete with one another in some fashion to gain associative strength when they are com~unded together during conditioning (e.g., Mackintosh, 1975; Pearce & Hall, 1980; Rescorla & Wagner, 1972). This assumption has been challenged, however, by recent findings in aversion conditioning. This research was supported by Grant BNS 83-00803 from the National Science Foundation. We thank David Baker, Ronald Gelb, and Andrew Lundeen for their work on related aspects of this project, Jed Marshall for keeping us supplied with Schilling almond extract from the West Coast, and Michael Fanselow for his comments on an earlier draft of the manuscript. Send correspondence and reprint requests to Mark E. Bouton, Department of Psychology, University of Vermont, Burhngton, VT 05405. 0023-%~/86

$3.00

Copyright 0 1986 by Academic Press, iac. All rights of reproduction in sxxy form reserved.

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When rats receive a taste and odor presented together during conditioning, the presence of the taste may facilitate, or “potentiate,” the conditioning of an aversion to the odor (e.g., Coburn, Garcia, Kiefer, & Rusiniak, 1984; Durlach & Rescorla, 1980; Lett, 1984; Palmerino, Rusiniak, & Garcia, 1980; Rusiniak, Hankins, Garcia, & Brett, 1979; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982; Westbrook, Homewood, Horn, & Clarke, 1983; see also Kucharski & Spear, 1985). Because taste does not interfere with, but instead facilitates, the conditioning of odor, potentiation is inconsistent with the interelement competition assumption made by most theories of compound conditioning. Odor potentiation by taste was originally reported by Rusiniak et al. (1979), who found that when saccharin was mixed with a solution containing almond extract, the saccharin taste potentiated the conditioning of almond (see also Durlach & Rescorla, 1980; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982). Rusiniak et al. (1979) argued that the almond cue was an olfactory stimulus even though the rats drank it: When rendered anosmic by pe~usion of the nasal mucosa with zinc sulfate, the rats lost their aversion to almond. Rusiniak et at. suggested that taste may potentiate odor because the two types of stimuli have qualitatively different, and nonredundant, functions in the ingestion sequence. Taste is a proximal cue that controls the consumption of foods, while odor is a distal cue that controls approach to foods. Although other investigators have found that taste may also potentiate the conditioning of other types of potentially distal cues in rats, including visual (Galef & Osborne, 1978), environmental (Best, Brown, & Sowell, 1984), and auditory cues (Ellins, Cramer, & Whitmore, 198% the conditions that permit potentiation to occur are not well understood at present. The results of at least four series of studies suggest that potentiation is not an inevitable consequence of compounding an odorant mixed in drinking water with a taste during aversion conditioning (Bouton & Whiting, 1982; Ida, 1984; Mikulka, Pitts, & Philput, 1982; Rosellini, DeCola, & Lashley, 1981). These investigators never observed odor potentiation by taste, even though they looked for it over a range of experimental conditions. Instead, they often found precisely the opposite result: Taste often attenuated, or overshadowed, the conditioning of odor (Bouton & Whiting, 1982; Mikulka et al., 1982). Such results question the generality of the potentiation effect, and suggest that potentiation is controlled by some set of variables that has not been isolated yet. The present experiments begin to identify some of the variables that distinguish the conditions that produce potentiation and overshadowing. We began by investigating an alternative method for presenting odor that was introduced by Palmerino et at. (1980). These investigators presented almond extract on a disc, or cup, near the location of the drinking spout. When saccharin was available from the spout, saccharin potentiated the

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conditioning of the almond cup odor. Our own original work with the almond cup odor yielded equivocal results: Although the odor aversion was not potentiated by saccharin, perhaps s~gni~cantly, it was not overshadowed either (Bouton & Whiting, 1982, Experiment 6). However, in the absence of any identifiable change in procedure, our subsequent studies with the cup odor have replicated the potentiation result of Palmerino et al. On the other hand, we have continued to observe overshadowing when the same odor-ant is mixed in the drink. The purpose of the present experiments was to document this difference in the properties of our cup and drink odors, and to begin the process of analyzing why it occurs. Experiments 1 and 2 established that the cup odor is potentiated by saccharin, and that the drink odor is overshadowed, when the two types of odors are conditioned and tested under identical conditions. The results of those experiments also suggested that the cup odor is a more effective distal cue than the drink odor when that effectiveness is indexed by the odor’s ability to suppress approach to the location of the drinking spout. Experiments 3 and 4 were then designed to examine the role of this difference, and the role of a difference in the conditionability of the two types of odors when they were paired with toxin alone, in the production of potentiation. EXPERIMENT 1 The first experiment examined the effects of saccharin on the conditioning of both almond cup and almond drink odors. Each type of odor was conditioned either alone or in compound with saccharin. For all groups, the odor was provided by Schilling brand almond extract, the odorant that is used in Garcia’s laboratory (e.g., Coburn et al., 1984; Palmerino et ai., 1980; Rusiniak et al., 1979; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982). Two pairs of groups received the extract on a cup positioned behind the drinking spout. One pair received the conventional amount of extract on the cup (0.2 ml; see Coburn et al., 1984; Palmerino et al., 1980; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982); the other pair received a smaller amount (0.05 ml) to test the generality of the results. The final pair of groups received the extract mixed in drinking water in the 2.0% (v/v) concentration that is used in Garcia’s laboratory (Rusiniak et al., 1979; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Fo~hman, & Garcia, 1982). This solution is potentiated in Garcia’s laboratory, but overshadowed in ours (e.g., Bouton & Whiting, 1982, Experiments 2-4). The present experiment allowed a direct comparison of the cup and drink odors because the two types of stimuli were conditioned and tested under identical conditions. The strength of odor aversions has usually been indexed in the po-

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tentiation literature by monitoring the rat’s consumption of water in the presence of the odor. However, we supplemented the fluid consumption measure in the present experiment with observational data gathered by means of an instantaneous behavior-sampling technique (e.g., Altmann, 1974). Specifically, we monitored the degree to which the different odors suppressed approach to the location of the drinking spout. Any differences in the degree to which the various stimuli suppressed this distal behavior would be useful in an analysis of the difference between the cup and drink odors, Method

Subjects The subjects were 36 female Wistar rats bred at the University of Vermont. They were between 100 and 140 days old at the start of the experiment and were housed individually in standard stainless-steel cages in a room maintained on a 12:12 h 1ight:dark cycle. The experiment was conducted on consecutive days during the light portion of the cycle. Apparatus Conditioning and testing were conducted in a set of four “conditioning boxes” housed in a room several meters down the hall from the home colony room. Each box measured 16.5 x 31 x 22 cm. The ceiling and three walls of the chamber were constructed of wood (painted white); one of the long walls was clear acrylic plastic, which permitted a clear view of the rat within the box. The floor was composed of 3-mm brass rods spaced 1 cm apart. Solutions were delivered through a standard stainless-steel spout (Girton) that extended 1.5 cm through a heavy rubber cup (3.5 cm in diameter and 2 cm deep) embedded in the right side wall. The opening in the end of the spout, through which the animals obtained fluid, was 3 mm in diameter. The cup was covered by a fine wire mesh. A piece of filter paper, 3 cm in diameter, was mounted on the inside of the cup, surrounding the spout. Cup odors were provided by placing either 0.2 or 0.05 ml of Schilling almond extract on the filter paper immediately prior to running the animal in the box. At all other times, the filter paper was dry; it was replaced, and the box was wiped with a moist sponge, prior to running each animal. The almond drink was provided by mixing the Schilling extract in distilled water in a concentration of 2.0% (v/v). Our human senses, as well as the data reported by Rusiniak et al. (1979), suggest that this solution is olfactory. When presented, the saccharin taste was provided by a 0.1% (w/v) saccharin solution mixed in distilled water. When compounded with a cup odor, the saccharin solution was available from the spout instead of distilled water. When compounded with the drink odor,

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both almond and saccharin were mixed in distilled water in a manner that preserved the individual concentrations. Procedure Drink training. The rats were initially trained to drink in the conditioning boxes over a series of nine daily lo-min drink sessions. The rats were water-deprived except for the IO-min drink in the conditioning box and a second lo-min drink in the home cage approximately 60 min later. Food was available on an ad libitum basis in the home cage, but was removed prior to the first drink and returned following the second. The animals were weighed each day prior to their transport to the conditioning boxes. conditioning. Following drink training, the animals were assigned to six groups (n = 6) so as to match the groups on their mean intake in the conditioning boxes over the final 3 days of drink training. Conditioning was then conducted over the next 6 days. On Days 1 and 4, the rats received experimental stimuli while they drank during the accustomed 10 min in the conditioning boxes. They were then immediately returned to the home cage. Thirty minutes later, each rat was injected intraperitoneally with a 5 ml/kg dose of a 0.6 M lithium chloride solution. Water was made available for 10 min in the home cage 90 min following the injection. The groups differed only in the stimuli they received in the conditioning boxes on these days. Groups Drink A, LoCup A, and HiCup A received the almond odor alone, either in the drink or on the cup in its low or high intensity, respectively. Groups Drink AS, LoCup AS, and HiCup AS received the corresponding almond stimuli in compound with saccharin. The rats were run in squads of four composed of two rats each from an A and an AS group. To prevent the influence of the possible airborne spread of odors between animals from different groups, the groups were run separately in the sequence of Drink, LoCup, and HiCup. Days 2, 3, 5, and 6 were water recovery days in which the rats were given distilled water in the conditioning boxes and the colony room using the procedure followed during drink training. Testing. Testing was conducted on the 5 days that followed the conditioning phase. On each of these days, each rat was tested for its aversion to the odor alone. Testing was conducted with a procedure identical to that used in conditioning, except that no lithium was administered. For each rat, the odor was presented with the same method that had been used during conditioning. As usual, each experimental session in the conditioning box was followed 60 min later by 10 min of water in the home cage. Dependent variables. Throughout the experiment, the strength of the aversion was measured by the amount of fluid each rat consumed in the presence of the experimental stimuli. However, during the final drink-

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training session, the two conditioning sessions, and during test sessions 1,2, and 5, an experimenter also observed the animals in the conditioning boxes and time-sampled their behaviors at 15-s intervals. An instantaneous scan sampling method (Altmann, 1974) was used in which, at the predetermined instants, the observer scanned each of the four rats that were run concurrently. The behavior of each was coded as either “near” to or “far” from the location of the odor. “Far” was defined as any behavior that occurred with three of the rat’s paws on the half of the box, marked by a vertical line on the rear wall of the box, opposite to the location of the cup and spout. During the second test session, two observers independently recorded the behavior of 16 animals. Interobserver agreement was 96.35%. Data analysis. The results of the present series of experiments were analyzed by means of analyses of variance (ANOVAs). In factorial experiments that were designed to compare the effect of saccharin on the conditioning of different types of odors (Experiments 1 and 4), pairwise comparisons were specified a priori and conducted in addition to the overall ANOVA; those comparisons were conducted with the distributionfree Mann-Whitney U test in cases where the overall ANOVA’s assumption of homogeneity of variance was threatened by group means of zero. Statistical analyses of test data ordinarily focused on the first test trial, except in cases where group differences were initially obscured by floor effects. The rejection criterion throughout was p < .OS; p values of less than . 10 were considered marginally significant. Results Consumption. The amount of fluid consumed by the groups in the presence of the experimental stimuli during conditioning and testing is shown in Fig. 1. Differences in consumption were present on the first LO CUP

HI CUP

12-

12 p-

COND.

TEST

COND.

TEST

A -0

10

AD

COND.

TEST

TRIALS

FIG. 1. Mean consumption during the conditioning and test trials of Experiment 1. The groups that received conditioning and testing with the 2.0% drink, the low-intensity cup, and the high-intensity cup are shown separately.

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conditioning trial, where a 3 (odor type) x 2 (compound factor) ANOVA revealed reliable main effects of both the odor type, F(2, 30) = 5.08, and compound, F(1, 30) = 6.90, factors; the odor x compound interaction was not reliable, F(2, 30) < 1.0. The reliable compound main effect agrees with other reports indicating less initial consumption with odortaste compounds than with odors presented alone (e.g., Bouton & Whiting, 1982; Rusiniak et al., 1979). To analyze the nature of the odor main effect, post hoc comparisons were conducted with Newman-Keuls tests; these revealed reliably less consumption in the presence of the drink odor than either cup odor, which did not differ reliably. Although every animal consumed some fluid on this trial, the results suggest that the drink odor initially suppressed consumption more strongly than either of the cup odors. The results of the test phase, when each odor was tested alone following conditioning, suggest that the different types of odors further varied in the strength of the aversions that became conditioned to them, and in the effect that saccharin had on their conditioning. An odor type x compound ANOVA was conducted on the mean consumption during testing because of the floor effects that were present initially. (It could be noted, however, that an ANOVA on the first test trial supported an identical set of conclusions.) The analysis revealed that saccharin generally potentiated the conditioning of odor, compound main effect F(1, 30) = 21.87, but that this effect depended largely on the type of odor, interaction F(2, 30) = 5.98. The overall difference in consumption in the presence of the various odors was also significant, odor main effect F(2, 30) = 15.87. Because the drink groups’ near-zero consumption during testing threatened the ANOVA’s assumption of homgeneity of variance, a priori pairwise comparisons were conducted with the Mann-Whitney U test. These comparisons confirmed that saccharin potentiated the conditioning of the cup odors, but not the drink. Groups LoCup AS and HiCup AS both differed significantly from their controls, U(6, 6) < 4, but Group Drink AS did not, U(6, 6) = 17.5. In addition, the drink odor conditioned alone (Group Drink A) suppressed consumption more than either of the cup odors conditioned alone (Groups LoCup A and HiCup A), U(6, 6) < 1, which did not differ, U(6, 6) = 12. The test consumption results thus suggest that the drink odor was more strongly conditioned than the cup odors, and that its conditioning was less likely to be potentiated by the saccharin taste. Behavioral observations. The percentage of time that the groups engaged in behavior on the far side of the conditioning box, away from the location of the cup and drinking spout, is shown in Fig. 2 for the trials on which observational data were taken. An odor type X compound ANOVA on the first conditioning trial revealed no initial differences among the

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DRINK

LO CUP

612125

CONK

HI CUP

812125 TEST

COND.

TEST

COND.

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TRIALS

FIG. 2. Mean percentage of the behavior samples recorded as far from the location of the cup and spout in Experiment 1. The drink, low-intensity cup, and high-intensity cup groups are shown separately. “B” denotes a baseline trial on which no odor was present.

groups in far behavior, F values < 2.38. However, the observational data during testing, like the consumption data, revealed strong differences in the properties of the cup and drink odors. When the cup odors had been conditioned with saccharin, the presence of the odor alone during testing moved the rats to the far side of the box. The odor in the drink, on the other hand, evoked relatively little such far behavior. The data from the first test trial were analyzed with a 3 (odor type) x 2 (compound factor) ANOVA. The analysis revealed an overall difference in the amount of far behavior evoked by the different types of odors, F(2, 30) = 4.14, and an overall potentiating effect of saccharin, F(l, 30) = 6.86. The interaction between the odor type and compound factors that is clearly suggested by the figure was not statistically reliable, F(2, 30) = 1.20. However, the results of a priori pairwise comparisons strongly suggested that the effect of saccharin depended importantly on the type of odor. Although the cup odors evoked more far behavior when they had been conditioned in compound with saccharin than when they had been conditioned alone [F( 1, 30) = 5.11 for HiCup; F( 1, 30) = 4.10 for LoCup, p < .06], the difference between the groups conditioned with the drink odor did not approach statistical significance, F(1, 30) < 1.0. Thus, saccharin potentiated the far behavior evoked by the cup odors, but not the drink odor. Finally, although far behavior did not differ among the groups conditioned with the odors alone, F(2, 30) = 1.81, it did among the compound-conditioned groups, F(2, 30) = 8.87. NewmanKeuls tests comparing the compound-conditioned groups revealed reliably more far behavior with the HiCup than with the drink; far behavior in Group LoCup AS did not differ reliably from the other two groups.

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Overall, the behavioral observations suggest that potentiated cup odors, but not drink odors, suppress approach to the location of the drinking spout. Discussion

The results of this experiment suggest that the two cup odor intensities that were examined here did not differ in the strength of the aversions that became conditioned to them, or in the extent to which they were potentiated by saccharin. However, the cup odors differed from the drink odor in at least three respects. First, saccharin potentiated the conditioning of the almond cups, but had no appreciable effect on the almond drink. The present failure to find an effect of saccharin on the drink odor is probably due to the floor effect that was clearly present during testing. In a number of published (Bouton & Whiting, 1982) and unpublished experiments in which extinction testing was continued long enough to get comparable groups off the floor, we have consistently observed overshadowing of the present almond drink by the present saccharin taste. Extinction was terminated after five test trials here because we wished to conduct other tests with the drink-conditioned animals before the aversion had extinguished (Experiment 2A). The results of those tests (reported below) revealed that saccharin had indeed overshadowed the drink. Thus, it is safe to conclude that the present cup and drink odors differ substantially in the effect that saccharin has on their conditioning: While cup odors are potentiated, the drink odor is overshadowed by taste. The difference in the effect of saccharin on cup and drink conditioning may be related to two other differences between the stimuli that emerged in the present experiment. First, the consumption data suggest that the drink odor conditioned alone was a relatively easily conditionable cue: Two pairings of the drink with delayed toxin caused a robust and persistent aversion (see also Bouton & Whiting, 1982), whereas the same pairings caused a relatively weak aversion to the odor when it was presented on the cup. Although the drink odor’s apparent ease of conditioning was confounded with the degree to which it suppressed consumption on the first conditioning trial, unpublished work in this laboratory indicates that prolonged suppression of consumption like that observed here depends directly on pairings of the drink with LiCl. In fact, the strength of the unconditional reaction to a stimulus may vary directly with its conditionability (cf., e.g., Kaye & Pearce, 1984). The observation that the drink odor produced a relatively strong unconditional effect on consumption may be consistent with the view that the drink is a relatively easily conditionable stimulus. Other aspects of the results suggest that the cup and drink odors may also differ in the types of behavior they control once they become conditioned. Although the compound-conditioned cup odors acquired the

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ability to suppress approach to the location of the drinking spout, the drink odor did not do so significantly. The relative inability of the drink odor to suppress approach behavior contrasts markedly with its ability to suppress consumption. The overall pattern of results is consistent with the view that the cup odor is relatively effective as a distal cue controlling approach to the location of the spout (cf. Rusiniak et al., 1979), while the drink odor is relatively effective as a proximal cue controlling consumption. We will investigate an implication of this difference in Experiment 3, after first comparing the cup and drink odors further in Experiment 2. EXPERIMENTS

2A AND 28

The results of Experiment 1 suggest that the effect of saccharin on odor conditioning depends on whether the odor is presented on the cup or in the drink. However, because the rats were tested with the same type of odor that was administered during conditioning, the difference between cup and drink could be due either to a difference in what the rats learned during conditioning, or in how they performed in the presence of the odors during testing. Experiments 2A and B were designed to distinguish between these alternatives. Experiment 2A examined how rats react to a drink-conditioned odor when it is tested on the cup; Experiment 2B examined how rats react to a cup-conditioned odor when it is tested in the drink. If the animals learn about cup and drink differently, then mode of testing should be irrelevant; if they merely peform to cup and drink differently, then mode of conditioning should be irrelevant. Method Subjects and Apparatus

The subjects of Experiment 2A were the animals from Groups Drink A and Drink AS of Experiment 1. The subjects of Experiment 2B were 12 female Wistar rats, from the same stock as before, 150 days old at the start of the experiment. The apparatus, housing, and maintenance conditions were the same as those of Experiment 1. Procedure Experiment 2A. Following the conclusion of the test phase of Experiment 1, the animals in Groups Drink A and Drink AS received 1 day in which distilled water was consumed during the usual IO-min drinks in the conditioning boxes and home cage. Beginning on the next day, there were three daily tests of the Schilling almond extract, now placed on the cup in the amount administered to the former HiCup groups (0.2 ml). Testing was conducted with the procedure described in Experiment 1. Both fluid consumption and behavioral data were gathered during each of the test trials.

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Experiment 2B. The details of Experiment 2B’s procedure were the same as those of Experiment 1 except as noted. The animals were initially trained to drink in the conditioning boxes over seven daily lO-min sessions; a second lo-min drink in the home cage followed the first by 60 min. The rats were then assigned to two groups so as to match them on consumption in the conditioning boxes on the final 3 days of drink training. The groups then received two conditioning trials with the 0.6 M lithium chloride injection delayed by 30 min. Group A received 0.2 ml of the almond extract on the cup during both trials; distilled water was available from the spout. Group AS received the same extract on the cup, but the 0.1% saccharin solution was available from the spout. After the 2 water recovery days that followed the second conditioning trial, every rat was tested for its aversion to the 2.0% almond drink. There were four tests of the drink over four consecutive sessions. Both fluid consumption and observational data were gathered during each of the test trials. Results Drink-conditioned

odor tested on the cup. The results of Experiment

2A are presented in the left-hand DRINK-.

panels of Fig. 3, where the amount of CUP

CUP -

12 TEST

DRINK

3

4

TRIALS

3. Results of the test trials in Experiments 2A and 2B. The results of Experiment 2A, when the drink-conditioned odor was tested on the cup, are shown in the left-hand panels; the results of Experiment 2B, when the cup-conditioned odor was tested in the drink, are shown in the right-hand panels. FIG.

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water consumed during the tests of the almond cup and the percentage of time the rats engaged in far behavior are shown separately. As the figure suggests, although the groups’ consumption changed markedly over the course of testing, the drink-conditioned odor demonstrated overshadowing when tested on the cup. A group x trial ANOVA conducted on the consumption data revealed no reliable effect of group, E;(l, 10) = 2.80, but both a trial effect, F(2, 20) = 23.67, and a signi~cant group by trial interaction, 1;(2, 20) = 4.05. Simple effect analyses comparing the groups on each trial revealed that Group AS consumed reliably more fluid on trial 3 than Group A, F(1, 30) = 7.20; the differences on the other trials were not reliable, F(1, 30) < 2.51. The observational data suggest a similar conclusion, although a similar analysis on those data revealed only a significant effect of trial, F(2, 20) = 18.39; neither the Group effect nor the group by trial interaction were reliable, F values < 2.05. Cup-conditioned odor tested in the drink. During the first conditioning trial of Experiment 2B, the group presented with the cup odor alone did not differ from the group presented the cup-saccharin compound in either consumption (6.0 and 5.4 ml, respectively) or far behavior (25.7 and 36.5%, respectively), F(I, 10) < 1.0. The results of Experiment 2B’s test trials, when the cup-conditioned odor was tested in the drink, are presented in the right-hand panels of Fig. 3. As the figure suggests, the animals conditioned with the cup odor in compound with saccharin demonstrated potentiation when tested with the drink. A group x trial ANOVA on the consumption data revealed a reliable effect of group, F(1, 10) = 4.98, and a reliable effect of trial, F(3, 30) = 3.10. The group x trial interaction was marginally significant, F(3, 30) = 2.40, p < .lO. (A Mann-Whitney U test on the average consumption over testing confirmed the reliable group effect, U(6, 6) = 2.) A group x trial ANOVA on far behavior revealed a reliable effect of trials, F(3, 30) = 5.42, although neither the group effect, F(X, IO) = 2.58, nor the group x trial interaction, F(3, 30) = 1.46, was statistically reliable. Discussion The results of this experiment suggest that aversions conditioned with one method of odor administration generalize substantially to tests conducted with the other. To some extent, that generalization may also include the ability of the conditioned odor to evoke far behavior: The cup-conditioned odor continued to evoke some far behavior when tested in the drink. More important, the consumption results suggest that the type of odor administered during conditioning is critical in determining potentiation and overshadowing. Regardless of the method used during testing, saccharin potentiated the cup-conditioned odor and overshadowed

COMPOUND ODOR CONDITIONING

the drink. The rats appear to learn differently drink odors. EXPERIMENT

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with the present cup and

3

Rusiniak et al. (1979) suggested that taste may potentiate, rather than overshadow, odor because odors and tastes guide different phases of the ingestion sequence. Because taste is a proximal cue that controls the consumption of foods, while odor is a distal cue that controls approach, the two types of stimuli are functionally nonredundant. The present results may be compatible with this view. The observational data of Experiment 1 confirmed that the compound-conditioned cup odor may function as a distal cue; it acquired the ability to suppress approach to the location of the drinking spout. The drink odor, in contrast, did not do so significantly; instead of suppressing approach, it primarily suppressed consumption. This pattern of results suggests the possiblity that saccharin may overshadow the drink odor because the drink is a redundant proximal cue. Experiment 3 was designed to investigate predictions that follow from this analysis. If potentiation results from the compounding of distal and proximal cues, and if the present proximal drink is redundant in function to the saccharin taste, then the proximal drink odor would be expected to potentiate the conditioning of a different distal odor. The present experiment was therefore designed to test the effect of the almond drink on the conditioning of a new strawberry cup odor. Pilot experimentation had established that the strawberry cup odor is discriminably different from the almond odor in that an aversion conditioned to almond did not generalize to strawberry. But like the almond cup, strawberry is both potentiated by saccharin and comes to suppress approach to the drinking spout. In the present experiment, the strawberry odor was conditioned alone, or was compounded with saccharin, the almond drink, or the almond cup during conditioning. If potentiation occurs when a proximal cue is compounded with a distal cue during conditioning, then both saccharin and the almond drink should potentiate strawberry. And if overshadowing occurs when redundant members of the same functional class are compounded during conditioning, then the distal almond cup odor might overshadow strawberry. Method Subjects and Apparatus

The subjects were thirty-two 120-day-old female Wistar rats obtained from the same stock as those in the previous experiments. Housing and maintenance conditions were also the same. The apparatus was the same as well, except that stainless-steel cups replaced the rubber cups, embedded in the wall of the conditioning boxes, that were used in the preceding

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experiments. The new cups were 4.5 cm in diameter and 3 cm deep; they were covered with hardware cloth. The filter paper on which the odorants were placed was positioned at the back of the cup and was 4.5 cm in diameter. The apparatus remained the same in all other details. As before, the drinking spout extended 1.5 cm out of the cup. Procedure

The procedure was the same as that of the previous experiments except as noted. After an initial 1 l-day drink-training phase, the rats were assigned to four groups (n = 8) so as to match the groups on mean intake in the conditioning boxes during the last 3 days of drink training. Two conditioning trials were then conducted over a 6-day phase as in the previous experiments. All groups received 0.2 ml of Durkee brand strawberry extract placed on the filter paper in the cup during the conditioning trials; the groups differed only with respect to the stimuli they received together with strawberry on these trials. Group St (strawberry alone) received distilled water at the spout; Group StS (strawberry-saccharin compound) received the 0.1% saccharin solution at the spout; Group StD (strawberryalmond drink compound) received the 2.0% almond solution at the spout; and Group StC (strawberry-almond cup compound) received distilled water at the spout and 0.2 ml of the almond extract (in addition to the strawberry) on the cup. After the customary 2 water-recovery days that followed the second conditioning trial, all groups were tested for their aversions to the strawberry cup odor alone. There were three test trials conducted on consecutive days. Both consumption and observational data were gathered on each of the conditioning and test trials. Results The groups’ consumption during conditioning and testing, as well as the percentage of time they engaged in far behavior, is presented in Fig. 4. One-way ANOVAs conducted on the data from the first conditioning trial revealed no reliable differences among the groups in far behavior, F(3, 28) = 1.74, but a marginally significant difference among the groups in fluid consumption, F(3, 28) = 2.73, p < .07. Although the figure suggests a strong trend toward lower consumption in the groups that received strawberry in compound with either saccharin (Group StS; cf. Experiment 1) or the almond drink (Group StD), post hoc comparisons with the Newman-Keuls test revealed no group differences that approached statistical reliability. Significant differences among the groups did emerge, however, during the tests of strawberry alone following conditioning. Like the almond cup odor, the strawberry cup was a weak cue for poison when it was conditioned alone (Group St). And when it was conditioned in compound with saccharin, conditioning of strawberry was potentiated (Group StS).

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FIG. 4. Mean consumption the groups during conditioning

(upper panel) and percentage far behavior (lower panel) of and testing in Experiment 3.

However, in contrast with saccharin, neither the almond drink odor (Group StD) nor the almond cup odor (Group StC) produced a significant effect on the strength of the aversion that was conditioned to strawberry. These impressions were confirmed by statistical analyses of both consumption and far behavior. A one-way ANOVA on consumption during the first test trial revealed a reliable difference among the groups F(3, 28) = 4.82. Newman-Keuls tests revealed that Group StS drank significantly less than Group St, indicating potentiation of strawberry by saccharin. Group StD, which had the almond drink compounded with strawberry, did not differ from Group St, but had a reliably weaker aversion than Group StS. Thus, the effect of the almond drink was quite different from that of saccharin. Group StC’s aversion to strawberry did not differ from that of either Group StD or Group St, but was marginally weaker than that of Group StS (p < .lO). A similar analysis on far behavior during the first test trial supported the same set of conclusions. The overall difference among the groups was reliable, F(3, 28) = 3.84; Newman-Keuls tests revealed that Group StS showed more far behavior than each of the other groups, which did not differ from one another. Saccharin thus potentiated both the consumption-suppressing and far behavior-evoking effects of the strawberry odor, while neither the almond drink nor the almond cup had an appreciable effect on either.

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Discussion The results of this experiment suggest that the properties of the strawberry cup odor are similar to those of the almond cup odors examined in the previous experiments. Strawberry was a relatively weak cue for poison when conditioned alone, its conditioning was potentiated by saccharin, and although its effect on far behavior was less dramatic than that of the almond cup, it similarly suppressed approach to the spout when it was conditioned in compound with saccharin. Although these observations suggest that the strawberry and almond cup odors may be considered redundant distal cues, the present experiment cannot determine whether such stimuli interfere with the conditioning of one another, because virtually no aversion was produced when strawberry was conditioned alone with the procedure that was used here. The most significant result of this experiment was the failure of the almond drink odor to potentiate the conditioning of strawberry. That failure suggests that the proximal almond drink is not a functional substitute for the saccharin taste. This observation suggests at least three further conclusions about the results up to this point. First, potentiation may not be the inevitable result of compounding stimuli, during aversion conditioning, that appear to function as distal and proximal cues. Second, since the almond drink and saccharin both appear to be easily conditioned, potentiation also does not appear to be a simple consequence of compounding a strongly conditionable cue with a weakly conditionable target. And third, the fact that the almond drink and the saccharin taste had such dissimilar effects on the conditioning of strawberry may argue against the possibility that the rats are able to taste the present almond drink. This inference agrees with the impressions of our human senses and the results of Rusiniak et al. (1979) suggesting that rats made anosmic lose their aversion to the same drink. The saccharin taste appears to be uniquely able to potentiate the conditioning of cup odors. EXPERIMENT 4 Another difference between the almond cup and drink odors, besides their possible status as distal and proximal cues, is that the cup is more difficult to condition when the stimuli are conditioned alone (Experiment 1). It is possible that saccharin may potentiate relatively weakly conditionable cues, but not relatively strong cues. Experiment 4 examined this possibility by diluting the concentration of the almond drink so that it was a weakly conditionable stimulus. The almond concentrations examined were 0.005 and 0.01% (v/v). Such weak solutions, which are 1/4OOth and 1/200th the concentration used in the preceding experiments, were suggested by pilot work which indicated that radical reductions in the concentration were required if the drink was to be conditioned as weakly as the cup. If weak cues for poison are potentiated by taste,

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then weakening the otherwise its ability to be potentiated.

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drink odor might improve

Method Subjects and Apparatus

The subjects were 24 female Wistar rats, obtained from the same stock as before, that were 130 days old at the start of the experiment. Housing and m~ntenan~ conditions were the same as in the preceding experiments; the apparatus was that used in Experiment 3. Procedure

The procedure was the same as before except as noted. Following 6 days of initial drink training, the rats were assigned to four groups (n = 6) so as to match the groups on consumption in the conditioning boxes on the final 3 days of drink training. Conditioning then began using the procedure described previously. The groups differed only in the drinks that were available from the spout during the conditioning trials. Two groups received a 0.005% solution of Schilling almond extract mixed in distilled water; the other two groups received a 0.01% solution. One of the groups conditioned with each concentration received the almond solution alone; the other group received the almond mixed with 0.1% saccharin. As usual, the compounds were constructed so as to preserve the individual concentrations. Following the 2 water days that followed the second conditioning trial, the groups received three tests of the almond solution alone. The test trials were separated by days in which only distilled water was consumed. For each rat, the concentration of the solution tested was the same as that conditioned. Systematic behavioral observations were not taken in the present experiment, because the results of the previous experiments indicated that the drink produces little far behavior. That suggestion was confirmed by our informal observations. Results The results of each of the conditioning and test trials are presented in Fig. 5. On each trial, consumption was expressed as a proportion of the amount consumed in the conditioning box on the immediately preceding “baseline” water day. This method of expressing the results was used because the groups differed in their baseline water consumption following conditioning. (During the water-recover day that preceded the first test trial, Groups .005A, .005AS, .OlA, and .OlAS drank 9.8, 14.0 10.8, and 11.8 ml in the conditioning boxes, respectively; comparable differences had not been observed in the preceding experiments.) Although the pro-

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5. Mean proportion of baseline consumption during the conditioning and test trials of Experiment 4. Groups conditioned and tested with the 0.005% almond drink solution are shown at left; the groups administered the 0.01% solution are shown at right. FIG.

portion measure increased the power of the present statistical analysis, the results were otherwise consistent when raw consumption was analyzed. The data from the first conditioning trial were analyzed with a 2 (almond concentration) x 2 (compound factor) ANOVA, which revealed a marginally reliable effect of compound, F(1, 20) = 4.24, p < .06, but no effect of concentration or a compound x concentration interaction, F( 1, 20) < 1 .O. The pattern of less consumption with the present compound stimuli is consistent with the pattern observed in the preceding experiments, as well as previous work on potentiation and overshadowing (e.g., Bouton & Whiting, 1982; Rusiniak et al., 1979). The data from the first test trial were also analyzed with a concentration x compound ANOVA, which revealed a marginally reliable main effect of concentration, F(1, 20) = 4.18, p < .06, and a reliable main effect of the compound factor, F(1, 20) = 8.57. The compound main effect suggests that saccharin potentiated the conditioning of the almond drinks used in the present experiment. The interaction between the concentration and compound factors suggested by the figure fell short of statistical reliability, F( 1,20) = 1 SO. However, a priori comparisons of the groups conditioned with each almond concentration indicated that while conditioning of the 0.005% solution was reliably potentiated by saccharin, F(1, 20) = 8.60, conditioning of the higher 0.01% concentration was not, F( 1, 20) = 1.45. The results thus suggest that potentiation of the almond drink is possible when extremely dilute solutions are used, and that the weaker the solution, the more likely this result obtains. Discussion

When the concentration of the almond drink odor was diluted substantially beyond the concentration used in the previous experiments,

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the drink became a weakly conditionable stimulus, and saccharin potentiated its conditioning. The fact that drink was potentiated after dilution suggests that the difference in the susceptibility to potentiation of the previous cup and drink odors may depend on quantitative, rather than qualitative, differences between the two: The conventional drink is a much stronger cue for poison than the cup. The present results suggest that saccharin may be especially likely to potentiate the conditioning of weakly conditionable cues. GENERAL DISCUSSION The results of the present series of experiments suggest that stimuli may differ widely in their abilities to be potentiated, and act as potentiators, in compound aversion conditioning. Although a strongly conditionable drink odor was overshadowed by saccharin (Expe~ment 2), weakly conditionable cup and drink odors were potentiated by the same stimulus (Experiments l-4). And although the saccharin taste served as an effective potentiator when compounded with several targets, neither the almond cup odor nor the almond drink odor potentiated the conditioning of an effective target (Experiment 3). The present experiments thus begin to identify some of the factors required for potentiation in compound aversion conditioning. The results of Experiments 1 and 2 suggest that the method used in administering odor is important in determining potentiation. When the odorant was presented on a cup near the location of the drinking spout, saccharin potentiated odor; but when it was mixed in the drink, saccharin overshadowed odor (Experiment 2; Bouton & Whiting, 1982; Mikulka et al., 1982; see also Ida, 1984; Rosellini et al., 1981). This difference between the cup and drink odors depended on their mode of presentation during conditioning; saccharin potentiated cup but overshadowed drink regardless of whether the odor was tested on the cup or in the drink (Experiment 2). The present difference between cup and drink odors is compatible with findings from other laboratories. In an experiment involving both almond cup and drink odors, Rusiniak, Palmerino, Rice, Forthman, and Garcia (1982; Experiment 1A) obtained results suggesting that the potentiating effect of saccharin was numerically larger with the cup odor than with the drink. Unfo~unately, because Rusiniak et al. did not report the interaction factor in their factorial analyses of variance, it is not possible to evaluate this comparison completely. However, Lett (personal communication, November 1983) has also used both methods of odor administration; her results suggested a trend toward overshadowing when almond was mixed in the drink (unpublished), but potentiation when it was presented on the cup (e.g., Lett, 1984). Potentiation may thus occur more readily with cup odors than with drink odors. Experiments 3 and 4 were designed to evaluate the roles of two other

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differences between the cup and drink odors in the production of potentiation. The results of Experiment 1 suggested that although the cup odor was effective as a distal cue that suppressed approach to the drinking spout, the drink odor was primarily effective as a proximal cue that suppressed consumption. In addition, the cup odor was a weaker cue for poison than the drink when the stimuli were conditioned alone. The results of Experiments 3 and 4 suggest that the classification of stimuli as distal and proximal cues may not be critical for an understanding of potentiation. In Experiment 3, the proximal almond drink failed to potentiate the conditioning of a different distal odor, which suggests that compounding stimuli that function as proximal and distal cues may not be sufficient to produce potentiation. And in Experiment 4, substantial dilution of the proximal almond drink allowed for potentiation by saccharin. The results of Experiment 4 suggest that the difference in the conditionability of the cup and drink may be the more important difference between them. Whether they were presented on the cup (Experiments l-3) or in the drink (Experiment 4). weakly conditionable cues were potentiated by saccharin. The observation that potentiation may depend on weak conditionability of the target is in general agreement with other findings. First, in experiments in which taste potentiated drink odors (Durlach & Rescorla, 1980; Rusiniak et al., 1979; Rusiniak, Palmerino, & Garcia, 1982; Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982), the drink odor appears to have been weakly conditioned alone when compared to other experiments in which taste overshadowed drink (Bouton & Whiting, 1982; Mikulka et al., 1982; see also Ida, 1984; Rosellini et al., 1981). The present experiments do not explain why drink odors in different laboratories differ so much in conditionability (recall that our almond drink is the same as that used in Garcia’s laboratory), but they suggest that odor conditionability may be a factor that distinguishes experiments yielding potentiation and overshadowing. Second, other cues that have been successfully potentiated by taste in rats, such as visual cues (Galef & Osborne, 1980), environmental cues (Best et al., 1984), and auditory cues (Ellins er al., 1985), are likewise only weakly conditionable when paired with toxin alone. Visual cues have also been potentiated by taste in pigeons and quail (Clarke, Westbrook, & Irwin, 1979; Lett, 1980, 1984), and it may be noted that these stimuli are also only weakly conditionable in these species when paired with poison alone. Finally, Palmerino et al. (1980) found that the potentiation of an almond cup odor was most likely with long CS-US intervals, which appeared to function primarily by weakening conditioning to the odor when it was conditioned alone. Under conditions in which the target stimulus is weakly conditioned, then, taste does appear to potentiate conditioning of the target. Although this conclusion appears to apply to a variety of findings, it

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may be appropriate to qualify it in at least two ways. First, there is evidence to suggest that weak conditionability of a target alone may not guarantee its potentiation. In an unpublished experiment, we were unable to produce potentiation of the 2.0% almond drink by exposing the rats to it repeatedly alone without lithium prior to conditioning. Preexposure made the drink odor only weakly conditionable, but it of course probably had other effects as well; for example, it could have reduced the odor’s ability to enter into an association with the taste during conditioning (cf. Durlach & Rescorla, 1980; Rescorla & Durlach, 1981, p- 98). On the other hand, Westbrook et al. (1983; Experiment 2) have reported data suggesting that a weakly conditionable odor may be overshadowed by taste if the compound is presented very briefly (for 2 min) during conditioning (in contrast, potentiation occurred when the compound was presented for 15 min). Although the overshadowed, shop-duration odor appeared only weakly conditioned when paired with toxin alone, it is worth noting that it was more strongly conditioned than its potentiated, longer duration counterpart. [In addition, Coburn et ~1. (1984) have reported potentiation, rather than overshadowing, with 2-min odor-taste compounds.] Although a detailed specification of the conditions that allow for potentiation still requires more experimental analysis, relatively weak target conditionability does appear to be a factor in the production of potentiation. As a second qualification, it should be recalled that the overshadowed drink odor in the present experiments was consumed less on the first conditioning trial than were the odors that were potentiated here (see Experiment 1). This observation opens the possibility that overshadowing and potentiation may depend on the amount consumed initially during conditioning, rather than on the target’s conditionability per se. However, it may be noted that, unlike our analysis of target conditionability, an analysis based on initial consumption levels would not predict that variables like the CS-US interval will affect the strength of potentiation (Palmerino et al., 1980). In addition, initial consumption levels did not predict potentiation in the present experiments very accurately. Overall, regardless of whether the compound yielded potentiation or overshadowing, the rats initially tended to consume less in the presence of the compound stimuli than they did in the presence of the odor(s) alone (see also, e.g., Bouton & Whiting, 1982; Rusiniak et al., 1979). Further, in Experiment 3 the saccharin taste successfully potentiated strawberry, while the almond drink did not, even though the strawberry-saccharin and strawberryalmond drink compounds were consumed in comparable amounts initially. These observations suggest that potentiation is not a simple function of initial consumption level. The overshadowed drink odor did produce a stronger unconditional effect on consumption than did the odors that

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were potentiated here, but that result may be consistent with the view that the drink is a relatively salient, and easily conditionable, stimulus. In a recent discussion of the contradictory outcomes obtained in previous odor-taste compound conditioning experiments, Coburn et al. (1984) noted that experimenters reporting the overshadowing of drink odors concomitantly found relatively strong conditioning with the odor alone. They further speculated that mixing an odorant in drinking water may add a potentiating taste component to the odor, and that the use of a hypertonic LiCl solution as the US (see Bouton & Whiting, 1982; Mikulka et al., 1982) may confound the illness produced by LiCl with pain produced by hypertonic intraperitoneal injections. [When a painful footshock is used as a US instead of illness in odor conditioning, saccharin may overshadow the conditioning of odor (Rusiniak, Palmerino, Rice, Forthman, & Garcia, 1982).] However, the present experiments did not confirm the speculations of Coburn et al. Potentiation was obtained here despite the use of a hypertonic LiCl solution as the US (see also Durlach & Rescorla, 1980; Lett, 1984). In addition, if the present almond drink had a taste component, that taste would presumably potentiate other odors besides the drink’s own odor component. The fact that the almond drink did not potentiate conditioning of the strawberry cup odor (Experiment 3) is inconsistent with this possibility. This observation, coupled with the previous results of Rusiniak et al. (1979) suggesting that rats made anosmic lose their aversion to the same solution, suggests that strong conditioning with the present drink odor may not be due to a hypothetical taste component. Although the present experiments do not explain the present drink odor’s salience as a cue for poison, they begin to suggest that the drink’s salience may account for its failure to be potentiated.’ Theories of odor potentiation differ in whether they assume that odortaste compounds obey the general laws of compound conditioning (Durlach & Rescorla, 1980; Rescoral & Durlach. 1981) or follow qualitatively different conditioning laws (e.g., Rusiniak et al., 1979; Palmerino et al., 1980). General models of conditioning have traditionally assumed that elements of compound conditioned stimuli compete with one another for conditioning, and that the weaker the salience of a cue, the more likely it will lose the competition to a stronger cue (e.g., Mackintosh, 1975; Pearce & Hall, 1980; Rescorla & Wagner, 1972). The present results, which suggest that weakly conditionable cues are especially likely to be potentiated, rather than overshadowed, are clearly inconsistent with these assumptions. It is possible that better general models of conditioning will ’ Cobum et al. (1984) also suggested that “those who failed to find potentiation Durlach and Rescorla (1980) in method and theory” (p. 818). It should be noted, that except for the use of a hypertonic lithium solution and one attempt to Durlach and Rescorla’s unique procedure (Experiment 5), Bouton and Whiting neither.

followed however, reproduce (1982) did

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eventually account for both overshadowing and potentiation by providing a more detailed account of the role of the target CS’s salience. But the present results also suggest that conditioned stimuli may still differ on dimensions that are independent of their salience or conditionability. Although the present 2.0% almond drink odor was comparable to saccharin in its conditionability, only saccharin potentiated the conditioning of a compounded odor (Experiment 3). That result may be consistent with the possibility that odors and tastes have qualitatively different properties in compound aversion conditioning. REFERENCES Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 42, 227-267. Best, M. R., Brown, E. R., & Sowell, M. K. (1984). Taste-mediated potentiation of noningestional stimuli in rats. Learning and Mofivation, 15, 244-258. Bouton, M. E., & Whiting, M. R. (1982). Simultaneous odor-taste and taste-taste compounds in poison-avoidance learning. Learning and Motivation, 13, 472-494. Clarke, J. C., Westbrook, R. F., & Irwin, J. (1979). Potentiation instead of overshadowing in the pigeon. Behavioral and Neural Biology, 25, 18-29. Coburn, K. L., Garcia, J., Kiefer, S. W., & Rusiniak, K. W. (1984). Taste potentiation of poisoned odor by temporal contiguity. Behavioral Neuroscience, 98, 813-819. Durlach, P. J., & Rescorla, R. A. (1980). Potentiation rather than overshadowing in flavoraversion learning: An analysis in terms of within-compound associations. Journal of Experimental Psychology: Animal Behavior Processes, 6, 175-187. Ellins, S. R., Cramer, R. E., & Whitmore, C. (1985). Taste potentiation of auditory aversions in rats (ruttus norveqicus): A case for spatial contiguity. Journal ofComparative Psychology, 99, 108-l 11. Galef, B. G., & Osborne, B. (1978). Novel taste facilitation of the association of visual cues with toxicosis in rats. Journal of Comparative and Physiological Psychology, 92, 907-916. Ida, M. (1984). An analysis of potentiation in flavor-aversion learning. Journal of Child Development, 20, 6-12. Kaye, H., & Pearce, J. M. (1984). The strength of the orienting response during Pavlovian conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 10, 90-109. Kucharski, D., & Spear, N. E. (1985). Potentiation and overshadowing in preweanling and adult rats. Journal of Experimental Psychology: Animal Behavior Processes, 11, 1534. Lett, B. T. (1980). Taste potentiates color-sickness associations in pigeons and quail. Animal Learning & Behavior, 8, 193-198. Lett, B. T. (1984). Extinction of taste aversion does not eliminate taste potentiation of odor aversion in rats or color aversion in pigeons. Animal Learning & Behavior. 12, 414-420. Mackintosh, N.J. (1975). A theory of attention: Variations in the associability of stimuli with reinforcement. Psychological Review, 82, 276-298. Mikulka, P. J., Pitts, E., & Philput, C. (1982). Overshadowing not potentiation in taste aversion learning. Bulletin of the Psychonomic Society, 20, 101-104. Palmerino, C. C., Rusiniak, K. W., & Garcia, J. (1980). Flavor-illness aversions: The peculiar roles of odor and taste in memory for poison. Science, 208, 753-755. Pearce, J. M., & Hall, G. (1980). A model for Pavlovian learning: Variations in the

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effectiveness of conditioned but not of unconditioned stimuli. Psychological Review, 87, 532-552. Rescorla, R. A., & Durlach, P. J. (1981). Within-event learning in Pavlovian conditioning. In N. E. Spear & R. R. Miller (Eds.), Znformafion processing in animals: Memory mechanisms (pp. 81-112). Hillsdale, NJ: Erlbaum. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64-99). New York: Appleton-Century-Crofts. Rosellini, R. A., DeCola, J. P., & Lashley, R. L. (1981). Overshadowing and potentiation of odor by taste: The role of stimulus saliency. Paper presented at the meeting of the Psychonomic Society, Philadelphia, PA. Rusiniak, K. W., Hankins, W. G., Garcia, J., &Brett, L. P. (1979). Flavor-illness aversions: Potentiation of odor by taste in rats. Behavioral and Neural Biology, 25, l-17. Rusiniak, K. W., Palmerino. C. C., & Garcia, J. (1982). Potentiation of odor by taste in rats: Tests of some nonassociative factors. Journal of Comparative and Physiological Psychology,

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Rusiniak, K. W., Palmerino. C. C., Rice, A. G., Forthman, D. L., & Garcia, J. (1982). Flavor-illness aversions: Potentiation of odor by taste with toxin but not shock in rats, Journal of Comparative and Physiological Psychology, 96, 527-539. Westbrook, R. F., Homewood, J., Horn, K., & Clarke, J. C. (1983). Flavour-odour compound conditioning: Odour-potentiation and flavour-attenuation. Quarterly Journal of Experimental Psychology, 35B, 13-33. Received July 8, 1985 Revised November 14, 1985