Learning and Motivation 41 (2010) 141–149

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Learning and Motivation

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Learned preference for a hedonically negative flavor isobserved after pairings with positive post-ingestionconsequences rather than with a palatable flavor

Felisa González *, David García-Burgos, Isabel de Brugada, Marta GilDepartment of Experimental Psychology and Physiology of Behavior, University of Granada, CampusCartuja s/n, 18071 Granada, Spain

a r t i c l e i n f o a b s t r a c t

Article history:Received 2 February 2009Revised 18 January 2010Available online 18 February 2010

Keywords:Conditioned flavor preferenceFlavor–taste learningFlavor–nutrient learningMedicine effect

0023-9690/$ - see front matter � 2010 Elsevier Indoi:10.1016/j.lmot.2010.01.004

* Corresponding author. Fax: +34 958 24 62 39.E-mail address: fgreyes@ugr.es (F. González).

In two experiments, thirsty rats consumed a compound of sucroseand a non-preferred flavor. In Experiment 1, a conditioned prefer-ence was observed in the experimental group when animals weretested both thirsty and hungry, but not when they were tested justthirsty. Animals in the control group, which experienced the flavorand the sucrose unpaired, never showed a preference. Experiment2 replicated the absence of a preference in the experimental groupwhen rats were tested thirsty, but provided evidence that a flavor–taste association had been formed during training. After condition-ing, sucrose was paired with LiCl in group Dev whereas it wasunpaired in group NonDev. The sucrose devaluation produced adecrease in CS preference in group Dev, and an increment in groupNonDev. Taken together, these results show that preference for anon-preferred flavor can be readily observed after pairings withthe positive consequences of the US (calories or absence of anexpected illness) rather than with a palatable flavor.

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Learned flavor preference often occurs after an initially neutral flavor has been paired with anunconditionally preferred one. This learning provides a means through which rats and people solvethe problem of selecting from a variety of potentially edible substances, allowing the formation ofnew preferences based on experience throughout the lifespan. Learned preferences have been inter-preted as an instance of Pavlovian conditioning, with the neutral flavor acting as the conditioned stim-ulus (CS), and the unconditionally preferred flavor as the unconditioned stimulus (US). Nevertheless,

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142 F. González et al. / Learning and Motivation 41 (2010) 141–149

the precise psychological mechanism underlying learned preferences remains to be specified (Dwyer,2005).

Two different associations have been proposed to account for the phenomenon (e.g., Capaldi, 1992;Fedorchak & Bolles, 1987; Sclafani & Ackroff, 1994): flavor–taste (F–T) and flavor–nutrient (F–N)learning. In flavor–taste learning, the critical association is between the target flavor and the sensoryproperties of the taste of the US which can, in turn, produce hedonic reactions when the US taste issweet. Flavor–nutrient learning is based on the motivational properties of the US generated by itspostingestive consequences (i.e., calorific intake). Several lines of evidence support the idea that theseassociations differ and could be independent of each other. For example, F–T preference is hardly everproduced when there is a delay between CS and US, whereas F–N preference can be readily observedover a delay (e.g., Sclafani & Ackroff, 1994). F–N learning seems to be independent of F–T learning,since rats develop a preference for a flavor paired with an unconditioned hedonically negative tastesuch as alcohol—whose consumption produces calorific intake—when they are hungry (Mehiel & Bol-les, 1988). The two kinds of learning also differ in their sensitivity to motivational state at the time oftesting. Whereas F–N preference is enhanced by a motivational shift to hunger, there is no evidence ofthis modulation on F–T learning (e.g., Fedorchak & Bolles, 1987; Harris, Gorissen, Bailey, & Westbrook,2000).

The aim of the following experiments was to assess the role of these two possible sources of ac-quired preference when a highly non-preferred flavor is used as CS. Previous unpublished data ob-tained in our lab using this kind of CS showed no evidence of a conditioned preference when ratswere trained and tested thirsty (González, Brugada, & Gil, 2006). First, we wanted to replicate this re-sult and also determine whether the absence of a preference under these conditions was due to a fla-vor–taste acquisition deficit or to some factor related to the expression of this learning. Second, wewondered if, in spite of the absence of a preference when animals were tested thirsty, rats learned thatthe CS signaled calorific intake. To achieve this, we also tested animals hungry.

In Experiment 1, we used a highly non-preferred CS which, on the basis of our previous results, weexpected not to produce a preference in non-food deprived animals, even after being paired duringtraining with a highly palatable taste such as that provided by a sucrose solution. Yet, the CS shouldbe preferred under hunger, as it would be a signal for a nutrient. That should not occur for animals inthe control group in which the flavor and the sucrose were presented unpaired. In Experiment 2, weevaluated whether the absence of a preference for the CS shown by thirsty rats in the experimentalgroup was due to either a deficit in the acquisition of flavor–taste learning or to a factor related tothe expression of this learning. In order to choose between these alternatives, we made use of theUS devaluation technique of pairing sucrose (i.e., the taste of the US) with illness. The US devaluationeffect—the decrease in preference for the flavor CS after US devaluation—should only be detected if aflavor–taste association was formed during training (i.e., if a flavor–taste association has been formed,the flavor will retrieve the representation of the taste associated with illness after the devaluation and,consequently, the preference for the flavor should decrease).

Experiment 1

This experiment made use of a CS that is not normally preferred by rats, an unsweetened 0.2% (2 g/L) Kool–Aid fruit-flavored solution in tap water. This solution at lower concentrations is often pre-sented in compound with saccharine to increase its acceptability (e.g., Myers & Sclafani, 2006). TheKool–Aid-solution concentration used here is 2–4 times higher than that used in other studies, butnot so high as to prevent an enhanced consumption under hunger using a one-bottle test (e.g., Bal-leine, Espinet, & González, 2005). The experiment was designed to maximize the opportunities of get-ting flavor–nutrient learning by giving extended exposure to the conditioning compound (eight trials)in group Simultaneous, and using a high sucrose solution concentration as the US (200 g/L). Animals ingroup Unpaired received the flavor and the sucrose at different times, one solution in the morning andthe other in the afternoon. After training, conditioned preference was assessed by two choice tests (fla-vor vs. water), one with animals thirsty, and the other with animals thirsty and hungry.

F. González et al. / Learning and Motivation 41 (2010) 141–149 143

Methods

Subjects and apparatusThe subjects were 16 female Wistar rats at least 110 days old at the start of the experiment. They

had previously participated in a flavor preference experiment with 1% (v/v) almond, 1% (v/v) vanilla,and sucrose (200 g/L), but were orthogonally assigned to both groups in order to equalize experiencewith these stimuli. Animals were housed in individual home cages and kept in a large colony room ona 12-h light/12-h dark schedule (light coming on at 7 am). All training sessions took place twice a dayin the home cage during the light cycle (approximately at 11 am and 5 pm), whereas tests were con-ducted during the morning session. Rats had continuous access to food throughout the experimentwith the exceptions mentioned below. They were maintained on a water deprivation schedule withdaily 30-min access to fluid (flavored solution or water). Fluids were administered at room tempera-ture in two 50-mL plastic tubes with a rubber stopper fitted with a stainless steel ball-bearing tippedspouts. Fluid consumption was measured by weighing the tubes before and after fluid presentation tothe nearest 0.1 g. The US was a 20% (200 g/L) sucrose solution, and the CS (flavor A) was a Kool–Aidcherry-flavored unsweetened solution at 0.2% (2 g/L) concentration. When flavor A and sucrose werepresented forming a compound, 200 g of sucrose and 2 g of Kool–Aid flavor were added to a liter ofwater. Fresh solutions were made every day using room temperature tap water.

ProcedureBefore the start of training, rats were water deprived for 4 days during which they had free access

to water for 30 min once a day during the morning session. Afterwards, they were divided into twogroups matched in water consumption (group Simultaneous, n1 = 8; group Unpaired, n2 = 8). On days1–8, group Simultaneous received a conditioning trial, during the morning session on days 2, 5, 7, and8, and during the afternoon session on days 1, 3, 4, and 6. In each session, the rats had access to 10 mLof flavor A mixed with sucrose solution for 15 min. Rats also received 10 mL of water in the alternativesession every day. Rats in group Unpaired received 10 mL of the sucrose solution for 15 min at thesame time of the day that group Simultaneous received the compound solution, and 10 mL of flavorA for 15 min at the same time of the day that group Simultaneous received water. This procedureequalized experience with the calorific US. On day 9, all animals had the conditioning test duringthe morning session in which they had access to two bottles for 15 min, one containing 20 mL of flavorA solution and the other 20 mL of water. The positions of the bottles (i.e., left and right) were coun-terbalanced by group and day. Animals received 10 mL of water for 15 min during the afternoon ses-sion. At the end of this session, food was removed from the cages. On days 10–12, animals received 90-min access to both water and food during the morning session. On day 13, another two-bottle testidentical to the conditioning test of day 9 was conducted, differing only in that all animals were alsofood deprived.

Results

For all the analyses, a significance level of p < .05 was adopted. Data were analyzed using repeated-measures analysis of variance (ANOVA) followed by simple main effects Tukey’s tests, where appro-priate. Two-tailed t-tests were used to evaluate data not involving multiple comparisons. Preferenceratios [volume of A/(volume of A + volume of water)] were calculated for each two-bottle test.

Conditioning phaseConsumption of the compound in group Simultaneous, and of both the sucrose and the flavor A

solutions in group Unpaired, was analyzed through three repeated-measures ANOVAs with day asthe factor. Consumption of the compound in group Simultaneous differed among days,F(7, 49) = 4.09. Post hoc Tukey’s tests revealed that consumption on day 2 was lower than on the otherdays, which did not differ among themselves (means: 7.77, 6.75, 8.83, 7.98, 9.37, 8.41, 8.95, and9.57 mL). Regarding consumption of the sucrose solution in group Unpaired, the ANOVA revealedno differences among days, F(7, 49) = 1.10 (mean: 9.52 mL). However, the ANOVA conducted on theconsumption of flavor A in this group showed differences among days, F(7, 49) = 16.47. Post hoc Tu-

144 F. González et al. / Learning and Motivation 41 (2010) 141–149

key’s tests confirmed that consumption on days 2, 5, 7, and 8—the days in which animals drank flavorA during the afternoon session—was significantly lower than that on days 1, 3, 4, and 6, probably be-cause they were less thirsty (means for 4 days were 6.92 and 5.10 mL, respectively).

Conditioning testsPreference ratios were analyzed through a mixed two-way ANOVA with group (Simultaneous, Un-

paired) as a between-subjects factor, and test (thirst, thirst plus hunger) as a within-subjects factor(see Fig. 1). The ANOVA revealed significant main effects of group, F(1, 14) = 12.15, test,F(1, 14) = 7.25, and the group � test interaction, F(1, 14) = 23.74. The t-tests revealed that groupsdid not differ on the test under thirst, t(14) = 0.65, but that they did differ on the test under both thirstand hunger, t(14) = 7.66. The preference in group Simultaneous was larger than the preference ingroup Unpaired. In addition, there was no change in preference in group Unpaired between tests,t(7) = 1.38, but preference increased in group Simultaneous on the test under thirst and hunger,t(7) = 6.12.

Discussion

The results from Experiment 1 are straightforward. Pairing a non-preferred flavor with sucrose didnot produce any evidence of a conditioned preference when animals were tested just thirsty. Prefer-ence ratios for both groups, Simultaneous and Unpaired, were virtually identical. One possible expla-nation for this lack of a difference between groups is generalization decrement from the compound tothe flavor in group Simultaneous. Rats might not recognize flavor A when presented separately fromthe compound. However, a conditioned preference in group Simultaneous was observed when animalswere also hungry, a finding that is at odds with the generalization decrement account. We concludedthat animals refused to drink flavor A in the first test when it was presented apart from sucrose be-cause they still found it aversive. Although the flavor did not become more palatable as a result oftraining, it could, none the less, become a cue associated with caloric intake. Under the assumptionthat animals will accept an unpleasant flavor associated with caloric intake when they are hungry,

Fig. 1. Experiment 1. Mean preference ratio (flavor A) for groups Simultaneous and Unpaired during the conditioning testsunder thirst (left side) and thirst plus hunger (right side). Group Simultaneous received eight flavor–sucrose compounds duringtraining while group Unpaired received flavor and sucrose several hours apart. Rats was water but not food deprived duringtraining. Error bars represent SEM.

F. González et al. / Learning and Motivation 41 (2010) 141–149 145

the motivational change introduced for the second test could have produced an increment in prefer-ence. If animals learned that flavor A was paired with caloric intake, and the motivational stateencouraged them to look for calories, flavor A could become a preferred fluid—hungry rats would con-sume a flavored solution as a function of the caloric value of the solution. On the other hand, if theywere not hungry but just thirsty, a non-palatable fluid that signals unneeded calories would beavoided when presented at the same time as water—under these conditions thirsty rats would con-sume a flavored solution as a function of the hedonic value of the solution.

Experiment 2

The absence of a preference for flavor A in the test given when the rats were just thirsty suggeststhat they really are averse to the flavor, even after it had been paired eight times with a strong sucrosesolution. Nevertheless, this result does not demonstrate that a flavor–sweetness (F–T) association wasnot formed during training. To address this issue we made use of the US devaluation technique inExperiment 2. Thirsty rats were trained under conditions similar to those used for group Simultaneousin Experiment 1, with the exception that they received two daily conditioning sessions over 4 days in-stead of a single conditioning session on each of 8 days. Afterwards, animals in group Dev (devalua-tion) received two cycles of sucrose–lithium chloride (LiCl) pairings before being tested underthirst, whereas animals in group NonDev received sucrose and LiCl unpaired. If a flavor–sweetnessassociation formed during training, a decrease in preference should be observed in group Dev butnot in group NonDev.

Methods

Subjects and apparatusThe subjects were 16 female Wistar rats at least 110 days old at the start of the experiment. They

had previously participated in a flavor preference experiment with 1% (v/v) almond and 20% (200 g/L)sucrose, but were orthogonally assigned to both groups in order to equalize experience with thesestimuli. They were housed and maintained under the same conditions as were used in Experiment1, with the exception that they were never food deprived. The US was again a 20% (200 g/L) sucrosesolution in tap water. The CS (flavor A) was this time a Kool–Aid artic-green-apple-flavored unsweet-ened solution in tap water at 0.2% (2 g/L) concentration. During the devaluation phase, animals re-ceived intraperitoneal (i.p.) injections of 0.15 M LiCl at 20 mL/kg of body weight.

ProcedureBefore the start of training, rats were water deprived for 4 days during which they had free access

to water for 30 min during the morning session. On days 1–4, animals received two daily conditioningtrials, one in the morning and the other in the afternoon. In each one, rats had access to flavor A mixedwith 20% sucrose solution for 15 min. No additional water was supplied in this phase. The condition-ing test occurred on day 5. Animals were given one 15-min two-bottle choice test (20 mL of flavor Avs. 20 mL of water) during the morning session, and 15-min access to water during the afternoon.They were also weighed at the end of the session. Rats were subsequently divided into two equal-sizedgroups matched in preference ratio. The US devaluation phase took place during days 6–11, in whicheither sucrose solution or water was presented in a single bottle. Animals in group Dev (n1 = 8) re-ceived two 2-day cycles of sucrose devaluation (days 6–9), and then a 2-day cycle of fluid consump-tion (days 10–11). On the first day of each sucrose devaluation cycle, rats were given access to 20 mLof sucrose solution for 15 min followed by an i.p. LiCl injection, while on the second day they received15 min access to water only. Animals in group NonDev were also injected with LiCl on the first day ofeach cycle, but they were given access to water instead of sucrose. On the second day, they had accessto 20 mL of sucrose for 15 min. Both groups received 15 min of water access in the afternoons. On days10–11, animals in group Dev drank sucrose on the first day and water on the second. Animals in groupNonDev drank water on the first day and sucrose on the second. Preference tests, identical to the con-

146 F. González et al. / Learning and Motivation 41 (2010) 141–149

ditioning test conducted on day 5, took place during the mornings of days 12–14. Animals were givenan additional 15 min of water access during the afternoons of days 12 and 13.

Results

Conditioning phaseCompound consumption in each of the morning and afternoon sessions was averaged to obtain a

daily value that was then analyzed (means: 6.83, 7.93, 8.80, and 9.09 mL). An ANOVA conducted overthe consumptions on the 4 days of training yielded a significant effect of day, F(3, 45) = 22.11. Pairwisecomparisons using Tukey’s test showed that consumption on days 1 and 2 differed from that on days 3and 4, but that day 1 did not differ from day 2 and that day 3 did not differ from day 4.

Conditioning testAfter this phase, animals were randomly divided into two halves and the preference ratios were

analyzed (Fig. 2, left side). Because there was no difference between the two subgroups,t(14) = 0.96, they formed the groups Dev and NonDev for the following phase (the mean preferenceratios were 0.28 and 0.35, respectively).

Devaluation phaseAn ANOVA on sucrose consumption during the 3 days of this phase with group and day as factors,

yielded main effects of both group, F(1, 14) = 35.47, and day, F(2, 28) = 5.20, and their interaction,F(2, 28) = 4.33. Post hoc Tukey’s tests showed that the average consumption of sucrose differed be-tween groups on day 3 (NonDev: 11.39, 10.35, and 10.89 mL; Dev: 9.07, 7.25, and 3.06 mL). Two sep-arate ANOVAs with day as factor, showed a significant effect of day in group Dev, F(2, 14) = 7.21, butnot in group NonDev, F < 1. Regarding differences in consumption in group Dev, Tukey’s tests showedthat the sucrose consumption on day 1 differed from that on day 3, and marginally from that on day 2(p = 0.05).

Fig. 2. Experiment 2. Mean preference ratio (flavor A) for groups Dev and NonDev on conditioning and three post-devaluationtests. Both consumed eight simultaneous flavor–sucrose pairings during training. Group Dev received two sucrose–LiCl pairingsafter conditioning, whereas sucrose and LiCl injections were unpaired in group NonDev. Error bars represent SEM.

F. González et al. / Learning and Motivation 41 (2010) 141–149 147

Preference tests after US devaluationMean preference ratios for flavor A after the devaluation phase for each group appear in Fig. 2 (right

side). Preference in group Dev seems to be much lower than in group NonDev. The ANOVA with groupand day as factors confirmed this impression, yielding a significant main effect of group,F(1, 14) = 28.64. No other main effect or interaction was significant. Although US devaluation mightbe expected to reduce preference in group Dev, it may be noted that the preference ratios shownby group NonDev are in fact quite high compared with that of the conditioning test. To test for this,an ANOVA with group and day (conditioning test vs. first devaluation test) as factors was conducted.The analysis yielded a significant main effect of group, F(1, 14) = 23.29, and a significant group � dayinteraction, F(1, 14) = 23.77. Mean comparisons in each group revealed that both groups changed pref-erence after devaluation. In group Dev, there was a significant decrease, t(7) = 2.74, whereas in groupNonDev the preference increased, t(7) = 3.99.

Discussion

Performance on the conditioning test in Experiment 2 was similar to that obtained in Experiment 1 forgroup Simultaneous when rats were tested thirsty, and thus replicates the absence of a preference. In or-der to detect a flavor–taste association, the taste of the US was devalued by pairing the sucrose solutionwith two i.p. LiCl injections in group Dev. A decrement in preference for flavor A, which remained throughthe three days of testing, was observed. This result proves that the absence of a preference in thirsty ratsis not due to a deficit in flavor–taste learning acquisition, and might be attributed to performance factors.The flavor–sweetness association could not be effective in producing a CS hedonic shift because theintensity of the unpalatable flavor was so high as to counteract the effect of the associate sweetness.Thus, rats preferred water to an unpalatable solution paired with calories when thirsty, and only showeda preference for the flavored solution when they were hungry (Experiment 1).

On the other hand, the high preference ratios shown by group NonDev after the devaluation phasewere rather surprising. Preference for a flavor increases when its consumption is paired with recoveryfrom illness (Green & Garcia, 1971). Although that was not exactly the case in this group—illness andsucrose were experienced 24 h apart—the alternation between the unpaired experiences of illness andsucrose could have promoted inhibitory learning. Sucrose could signal the absence of—rather than therecovery from—an otherwise expected illness. Since flavor A was paired with sucrose during trainingand a flavor–sucrose association formed, the increase in preference in group NonDev could be medi-ated by inhibitory learning. This possibility is further discussed in the next section.

General discussion

Taken together, the results of Experiments 1 and 2 show the absence of a conditioned flavor pref-erence in thirsty rats after simultaneous pairings of a highly non-preferred flavor (CS) and a nutrientwith a palatable taste (US). Nevertheless, the preference is observed when the positive consequencesof the US consumption are either relevant to the motivational state (Experiment 1) or have been en-hanced by means of a negative relationship with illness (Experiment 2).

In Experiment 1, relevance was achieved by a motivational change. Thirsty rats did not show anyevidence of a preference on the conditioning test. However, when rats were tested also hungry, thepreference ratio for the CS in group Simultaneous increased significantly over that shown by groupUnpaired, suggesting the existence of a flavor–nutrient association acquired during training. The factthat this preference was only observed when rats were hungry suggests that hunger modulates theexpression of learning acquired during conditioning (Harris et al., 2000; Yiin, Ackroff, & Sclafani,2005a, 2005b). Hunger may promote the consumption of a flavor paired with a nutrient even if theflavor is unpalatable.

Regarding Experiment 2, preference for flavor A decreased when its associate sucrose was pairedwith i.p. LiCl injections (group Dev), providing evidence of a CS-sweetness (i.e., flavor–taste) associa-tion formed during training. This association however was insufficient to produce a preference on theconditioning test, probably due to the initial low palatability of the flavor. On the other hand, prefer-

148 F. González et al. / Learning and Motivation 41 (2010) 141–149

ence for the CS increased after the devaluation phase in group NonDev, in which sucrose was pre-sented on the days when illness was absent. It is then possible that the sucrose-illness negative cor-relation promoted inhibitory learning, making sucrose a signal for the absence of illness, as well as itsassociate flavor A.

There is some evidence suggesting that a flavor paired with recovery from illness becomes pre-ferred, the so-called ‘‘medicine effect”. Green and Garcia (1971) found a preference for a fluid witha distinctive flavor consumed during the recuperation interval of an i.p. apomorhine hydrochlorideinjection, a drug that produces illness. Flavor enhancement has also been found using lithium chloridefor flavors consumed both 60 and 90 min after i.p. injections during 4 days (Hasegawa, 1981), as wellas 75 min after the injection during 8 days (Barker & Weaver, 1991; Experiment 1). Barker and Weaversuggested that conditioned preference through the ‘‘medicine effect” could be produced by condi-tioned inhibition because they found a retardation of conditioned aversion in the enhanced flavorgroup (Experiment 4).

The results of group NonDev in our study could be explained in a similar way if we assume that a24-h interval between the experiences of sucrose and illness supports inhibitory learning, and that fla-vor A, as an associate of sucrose, could act as an inhibitor as well. Regarding the first assumption, su-crose could become an inhibitor of illness because it is paired with the absence of—rather thanrecovery from—an expected illness. Inhibitory learning involving CS–US between-session negativecorrelation has been reported in a conditioned lever-pressing suppression experiment (e.g., Baker,1977). Regarding the second assumption, flavor A, as an associate of sucrose, could also become aninhibitor. As far as we know, this ‘‘medicine-like effect” involving an associate of the flavor that signalsthe absence of illness has not been previously reported. The association between flavor A and the fla-vor of sucrose may have promoted a ‘‘medicine-like effect” in at least two ways, both relying on thebidirectional association formed between flavor A and the taste of sucrose during simultaneous com-pounding in training. On the one hand, flavor A could recover the sucrose representation on testthrough the associative chain flavor A-sucrose-no illness. The other mechanism would be a ‘‘mediatedmedicine-like effect”. During the devaluation phase, sucrose could have recovered the representationof flavor A which would thus be active at the time the animal is experiencing the absence of an ex-pected illness. From some theoretical perspectives, the representations evoked by a stimulus can sub-stitute for the stimulus itself in the formation of new associations (Holland, 1981). The omission of theexpected illness in the presence of the activated representation of flavor A would endow it with inhib-itory properties, causing the increment in preference in group NonDev. Conditioned inhibition of anaversion has been related to increases in consumption/preference (Best, Dunn, Batson, Meachum, &Nash, 1985). Our results at the present moment do not allow us to decide which of these alternativesis correct.

Finally, we have to mention that the nature of the taste unpaired with illness could have signifi-cantly contributed to our results. Sucrose has an attractive taste and produces positive affective andmotivational consequences, all of which could have potentiated its properties as an inhibitor of thenegative state of illness. It remains to specify whether neutral stimuli have the same capacity to func-tion as an inhibitor, at least in just a few trials, and whether an associate could also show a medicine-like effect. Though interesting, those questions lie beyond the scope of the present study.

Taken together, the results of Experiments 1 and 2 suggest that, when using a hedonically negativeflavor, thirsty rats probably acquire both flavor–taste and flavor–nutrient learning during training.That a flavor–taste association was formed is shown by the US devaluation effect found in groupDev (Experiment 2). On the other hand, the increase in preference observed in group Simultaneous(Experiment 1) after a motivational change to hunger suggests that animals also formed a flavor–nutrient association. It is worth noting that rats seem to acquire flavor–nutrient learning in the ab-sence of explicit food deprivation, suggesting that this learning occurs after pairing a flavor withthe postingestive effects of sucrose, even if animals are not food-deprived during training (see alsoYiin et al., 2005a, 2005b). Finally, preference for a hedonically negative flavor can also be increasedby pairing it with a flavor which is negatively correlated with illness.

In summary, these results suggest that preference for a disliked flavor can indeed be induced bypairing it with positive post-ingestion consequences rather than with a palatable flavor. Giving a pal-atable flavor after the consumption of an unpalatable one often decreases rather than increases pref-

F. González et al. / Learning and Motivation 41 (2010) 141–149 149

erence for the unpalatable flavor, probably due to negative contrast (i.e., the ‘‘dessert effect”; see Cap-aldi (1996)). Giving simultaneous pairings of both flavors does not seem to be more effective in pro-ducing a conditioned preference for the unpalatable flavor when animals are just thirsty. Instead, theconditioned preference arises when the positive consequences of the US are enhanced after training bya relevant change in motivational state or by means of a negative relationship with illness.

Acknowledgments

This research was supported by CICYT Grant #SEJ2006-13851 (MEC, Spain), partially funded byFEDER funding, and Grant #HUM-02763 (Junta de Andalucía, Spain). The authors are grateful to Pro-fessor G. Hall and Professor William A. Roberts for their helpful comments on a previous version of themanuscript, F. Garzón for his assistance with the experiments, and Irin Evans for language editing ofthe manuscript.

References

Baker, A. G. (1977). Conditioned inhibition arising from a between-session negative correlation. Journal of ExperimentalPsychology: Animal Behavior Processes, 3, 144–155.

Balleine, B. W., Espinet, A., & González, F. (2005). Perceptual learning enhances retrospective revaluation of conditioned flavorpreferences in rats. Journal of Experimental Psychology: Animal Behavior Processes, 31, 341–350.

Barker, L. M., & Weaver, C. A. (1991). Conditioning flavor preferences in rats: Dissecting the ‘‘medicine effect”. Learning andMotivation, 22, 311–328.

Best, M. R., Dunn, D. P., Batson, J. D., Meachum, C. L., & Nash, S. M. (1985). Extinguishing conditioned inhibition in flavour–aversion learning: Effects of repeated testing and extinction of the excitatory element. The Quarterly Journal of ExperimentalPsychology, 37B, 359–378.

Capaldi, E. D. (1992). Conditioned food preferences. In D. Medin (Ed.). The psychology of learning and motivation (Vol. 28,pp. 1–33). New York: Academic Press.

Capaldi, E. D. (1996). Why we eat what we eat? Washington, DC: American Psychological Association.Dwyer, D. M. (2005). Reinforcer devaluation in palatability-based learned flavor preferences. Journal of Experimental Psychology:

Animal Behavior Processes, 31, 487–492.Fedorchak, P. M., & Bolles, R. C. (1987). Hunger enhances the expression of calorie-mediated but not taste-mediated conditioned

flavor preferences. Journal of Experimental Psychology: Animal Behavior Processes, 13, 73–79.González, F., Brugada, I., & Gil, M. (2006). Dissociation between the conditions of flavour–flavour and flavour–calories learning

in conditioned flavour preference. In Chemical senses, 31, E21 (meeting abstract). Poster session presented at the XVII annualmeeting of the European chemoreception research organization, Granada (Spain).

Green, K. F., & Garcia, J. (1971). Recuperation from illness: Flavor enhancement in rats. Science, 193, 749–759.Harris, J. A., Gorissen, M. C., Bailey, G. K., & Westbrook, R. F. (2000). Motivational state regulates the content of learned flavor

preferences. Journal of Experimental Psychology: Animal Behavior Processes, 26, 15–30.Hasegawa, Y. (1981). Recuperation from lithium-induced illness: Flavor enhancement for rats. Behavioral and Neural Biology, 33,

252–255.Holland, P. C. (1981). Acquisition of representation-mediated conditioned food aversions. Learning and Motivation, 12, 1–18.Mehiel, R., & Bolles, R. C. (1988). Learned flavor preferences based on calories are independent of initial hedonic value. Animal

Learning & Behavior, 16, 383–387.Myers, K. P., & Sclafani, A. (2006). Development of learned flavor preferences. Developmental Psychobiology, 48, 380–388.Sclafani, A., & Ackroff, K. (1994). Glucose-conditioned and fructose-conditioned flavor preferences in rats: Taste versus

postingestive consequences. Physiology & Behavior, 56, 399–405.Yiin, E., Ackroff, K., & Sclafani, A. (2005a). Flavor preferences conditioned by intragastric nutrient infusions in food restricted and

free-feeding rats. Physiology & Behavior, 84, 217–231.Yiin, E., Ackroff, K., & Sclafani, A. (2005b). Food deprivation enhances the expression but not acquisition of flavor acceptance

conditioning in rats. Appetite, 45, 152–160.