(CS) and the state of intoxication as unconditionedstimulus (US) (Deutsch & Eisner, 1977). Similarly,when high blood-alcohol levels result from rapid in-gestion of a distinctively flavored alcohol solution,the organism later rejects the sensory componentsof the experienced solution (Eckardt, 1975). Sucrose,sodium chloride, and saccharin solutions are avoidedafter paired presentations with intragastric or intra-peritoneal alcohol doses that range between 1.2 and5.15 g/kg (Berman & Cannon, 1974; Cordoba, Molina,Basso, & Orsingher, 1990; Lester, Nachman, & LeM-agnen, 1970).

Alcohol’s aversive unconditioned properties havealso been described in earlier stages of development.In weanling animals forced alcohol intake that ledto a clear behavioral state of intoxication not onlygenerated an aversion toward alcohol odor, but alsopotentiated previously learned aversions to the smellof alcohol that were originally established by pairingthis odor with lithium-induced toxicosis (Molina, Ser-watka, & Spear, 1984). Eleven-day-old pups learnedto avoid alcohol odor in a two-way olfactory locationaltest (Molina, Chotro, & Spear, 1989) and to avoid analcohol-containing solution in an intake assessment(Molina & Chotro, 1989a) after alcohol’s sensory at-tributes were experienced under a state of acute eth-anol intoxication that was achieved with an intragas-tric administration of a 3 g/kg alcohol dose (peakblood alcohol levels in this study were equivalent to260 mg%). During commencement of the third weekof postnatal life, rats readily associated the intraoralinfusion of sucrose solution with aversive uncondi-tioned properties of a 1.2 g/kg alcohol dose. Sucroseaversions have also been recorded when employingan alcohol dose equivalent to 0.4 g/kg but only underspecific state-dependent conditions: sucrose aver-sions were expressed only in organisms that experi-

121

1074-7427/96 $18.00Copyright 1996 by Academic Press, Inc.

All rights of reproduction in any form reserved.

NEUROBIOLOGY OF LEARNING AND MEMORY 66, 121–132 (1996)ARTICLE NO. 0053

Alcohol-Mediated Tactile Conditioned Aversions in Infant Rats:Devaluation of Conditioning through Alcohol-Sucrose Associations

JUAN CARLOS MOLINA, MICHELLE D. BANNOURA, M. GABRIELA CHOTRO, DAVID L. MCKINZIE, H. MOORE

ARNOLD, AND NORMAN E. SPEAR1

Department of Psychology and Center for Developmental Psychobiology, Binghamton University, Binghamton, New York 13902-6000

Three experiments were conducted to assess the plastic-ity of ethanol-mediated conditioned aversions to a tactilestimulus in infant rats. Ten- and 11-day-old rats first ac-quired an aversion to a texture, by virtue of its pairingwith alcohol-induced intoxication. This first conditioningphase was followed by an associative devaluation proce-dure, a second phase in which sucrose was intraorally in-fused during alcohol-induced intoxication. Pups were thentested for their texture preference. Results indicated thatinfant rats readily express conditioned aversion to a tactilecue as a result of tactile–alcohol pairings and that thisassociative learning was not state dependent. When alco-hol–texture conditioning was followed by sucrose–alcoholpairings, the magnitude of the texture aversion was dra-matically reduced (Experiments 1 and 2). In Experiment3 citric acid rather than sucrose was paired with alcoholintoxication following texture–alcohol pairings. The re-sults indicated that this procedure strengthened textureconditioned aversions in terms of increased resistance toextinction. Taken as a whole these studies indicate thatinfants rapidly acquire alcohol-mediated texture aversionsand that this memory is malleable and can be reduced orpotentiated through manipulation of the representation ofalcohol’s unconditioned properties. 1996 Academic Press, Inc.

It has been repeatedly reported that alcohol’s post-absorptive effects can act as an unconditioned stimu-lus that decreases intake of palatable substances pre-viously paired with the administration of the drug.Adult rats that are forced to drink this psychophar-macological agent have been observed subsequentlyto avoid alcohol’s odor or taste due to the associationbetween these sensory events as conditioned stimuli

1Address correspondence and reprint requests to Dr. NormanE. Spear, Department of Psychology, Binghamton University,Binghamton, NY 13902-6000

full

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enced a similar state of alcohol intoxication during a 2.0 g/kg dose of alcohol. Infants show a high prefer-ence for sucrose flavor (Hoffmann, Molina, Kuchar-both the acquisition and the testing phases of the

study (Hunt, Molina, Spear, & Spear, 1990). Further- ski, & Spear, 1987; Rozin & Zellner, 1985; Spear &Kucharski, 1984) and this flavor can act as an effec-more, conditioned aversions to milk have been de-

scribed in infant rats whenever consumption of this tive appetitive reinforcer in preweanling animals(Chotro, Cordoba, & Molina, 1991; Hunt et al. 1990;nutritional agent is followed by alcohol intoxication

(Alberts & Gubernick, 1984). Molina & Chotro, 1989a). Finally, infants were testedin a two-way texture preference test in which one ofAccording to the preceding information, infants

readily associate different CSs processed by the olfac- the alternatives was the tactile CS originally associ-ated with alcohol intoxication and the remaining cuetory and gustatory sensory systems with alcohol’s

aversive unconditioned properties. Such Pavlovian was a novel texture. The design allowed analysisof the following issues: (1) establishment of tactileconditioning can be analyzed in terms of associations

between the organism’s representations of events. aversions in infant rats as a function of texture–alcohol first-order conditioning procedures, and (2)One of these representations is related to the US.

Experiments have endorsed this hypothesis by dem- devaluation of the potential texture aversion whenthe first-order conditioning phase was followed byonstrating that when a CS–US association is estab-

lished, subsequent devaluation of the US component an acquired association between alcohol intoxicationand sucrose.will reduce the power of the CS to elicit the condi-

tioned response (Holland & Rescorla, 1975; Rescorla,1987). For example, if the US employed originally EXPERIMENT 1in the acquisition phase of the experiment was anappetitive stimulus, subsequent pairing of the origi- Methodnal US and an aversive US reduces response to theCS in comparison to controls not treated with the Subjectsdevaluation phase. In a recent study, it has been

Subjects were fifty-two 10-day-old Sprague–observed that these procedures yield a similar deval-Dawley-derived rat pups from our breeding colonyuation effect in 10-day-old pups (Kraemer, Hoff-at Binghamton University. Pups were representativemann, Randall, & Spear, 1992). Specifically, a condi-of 8 litters. The day of birth was designated Postnataltioned olfactory preference resulting from odor–heatDay 0 and litters were culled 24 h later (8–10 pupsassociations was devalued when the olfactory condi-per litter). Neonates were housed with both parentstioning phase was followed by heat–footshockand conspecifics in standard opaque maternity cages,pairings.partially filled with wood shavings. Water and Pur-In the present experiments ethanol-mediated con-ina Rat Chow were available ad libitum. The colonyditioned aversions were examined in a devaluationroom was maintained on a 16-h light/8-h dark illumi-procedure defined by the association between alco-nation cycle (light onset: 0600 h).hol’s aversive unconditioned properties and an appe-

titive reinforcer (sucrose solution). Experiments Apparatus and Procedureswere performed with infant rats subjected initiallyto a novel texture paired with acute alcohol intoxica- During Postnatal Day 10, pups were removed from

the home cage and quasi-randomly distributed to onetion. Recent preliminary research indicates that tex-ture cues paired previously with acute alcohol intoxi- of four groups. The sole constraint in the distribution

of pups was equivalent litter representation acrosscation are likely to elicit conditioned tactile aversions(Brasser, McKinzie, Molina, & Spear, 1993), similar groups. The four groups were defined by a factorial

design resulting from the experimental proceduresto alcohol-mediated conditioned aversions in infantanimals established with olfactory and/or gustatory employed in the two phases of the study [Phase 1:

Tactile conditioning phase in which a soft texturecues as CSs. One purpose of the present study wasto confirm and extend this conclusion. was explicitly paired (P) or unpaired (UP) with alco-

hol intoxication; Phase 2: Devaluation phase definedIn the first experiment of this study, pups experi-enced paired or explicitly unpaired presentations of by paired (P) or unpaired (UP) exposure to sucrose

infusion and acute alcohol intoxication]. Pups in thea novel texture and alcohol’s pharmacological effects.This first-order conditioning phase was followed by UP–UP condition (n = 13) received unpaired presen-

tations of the texture CS and alcohol intoxicationa second treatment phase in which pups were againsubjected to alcohol intoxication. In this phase a su- during the first phase of the experiment and subse-

quently were exposed to unpaired presentations ofcrose solution was explicitly paired or unpaired with full

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sucrose infusion and alcohol intoxication (Phase 2). trial per day). On each day following recordings ofbody weight, pups were placed into holding cagesUP–P pups (n = 13) received an explicitly unpaired

presentation of texture and alcohol intoxication separated in accordance with treatment condition.After the previously described 10 min of exposure to(Phase 1) followed by paired exposure to alcohol in-

toxication and sucrose infusion (Phase 2). P–UP sub- the soft texture CS they were returned to the holdingcages for an additional 20 min and then were re-jects (n = 11) received the texture CS paired with

the state of acute alcohol intoxication (Phase 1) and, turned to their biological parents. UP–UP and UP–Pgroups also experienced the soft CS and the 2.0 g/during Phase 2, were exposed to an unpaired expo-

sure comprising sucrose and alcohol intoxication. kg alcohol dose but in an explicitly unpaired manner.During Postnatal Days 10 and 11, these pups wereP–P (n = 15) animals experienced the tactile cue

explicitly paired with the state of intoxication (Phase placed in the soft texture for 10 min. Sixty minuteslater they were intubated with the alcohol US. The1) followed by paired exposure to alcohol intoxication

and sucrose infusion (Phase 2). To summarize, in overall time spent in the holding cages was keptconstant across all groups. All pups were returnedPhase 1 pups were exposed to paired or unpaired

presentations of a specific texture and alcohol, and to the maternity cages 1 h after being adminis-tered alcohol.in Phase 2 half of each of these groups were exposed

to paired presentations of alcohol and sucrose and Phase 2. On Postnatal Day 12 pups were removedfrom their biological parents and placed into holdinghalf to unpaired presentations.

Phase 1. Texture conditioning took place in clear chambers partially filled with wood shavings. Theywere orally cannulated using a procedure like thatPlexiglas chambers (8.5 × 25 × 20 cm). The floor of

these chambers was the soft side of a piece of stan- described in previous studies (Hunt et al., 1990, Mol-ina & Chotro, 1989a,b). Briefly, cannulae were madedard carpeting. Pups assigned to groups P–UP and

P–P experienced the soft CS texture while acutely with 5-cm sections of polyethylene tubing (Clay Ad-ams, PE 10, i.d. = 0.28 mm). One end of the sectionintoxicated with alcohol. Prior experiments have in-

dicated optimal sensitivity of measurement when the was heated in order to form a small flange. A pianowire attached to the nonflanged end of the tubing waspreferred (soft) texture is paired with an aversive

US (alcohol; e.g., Miller, Molina, & Spear, 1990). The placed on the medial internal surface of the cheek ofthe pup. The wire was then pushed through the oralalcohol dose was equivalent to 2.0 g of 95% ethanol

per kilogram of body weight (2.0 g/kg). This dose was mucosae until the flanged end of the cannula waspositioned over the internal surface of the mouthattained by intragastrically administering a volume

equivalent to 1.5% of the body weight of a 16.8% v/v while the remainder of the cannula exited from theoral cavity. These cannulae were later employed inalcohol solution. Pups in these groups were removed

from the maternity cage, weighed to the nearest 0.01 order to infuse a sucrose solution (15.3% w/v in tapwater) into the pup’s mouth. This sucrose concentra-g, and 60 min later intragastrically administered the

alcohol. Thirty minutes later they were individually tion has been observed to act as an appetitive rein-forcer in 11- to 12-day-old rats (Chotro et al., 1991).placed over the soft CS where they remained for 10

consecutive min. This pairing procedure has been For all animals, sucrose infusion lasted 10 min andwas performed with a pulsating rate (3 s on, 10 semployed previously in infant animals when examin-

ing ethanol-mediated conditioned aversions with oro- off). The infusion rate was calculated in order toachieve an overall infusion equivalent to 5.5% of thesensory or tactile cues (Brasser et al., 1993; Hunt et

al., 1990; Molina & Chotro, 1989a,b; Molina et al., preinfusion body weight of each rat. Infusion proce-dures were controlled with a Sage Instruments sy-1989). These previous tests have shown that with

the ages and doses used in the present study, presen- ringe pump (Model 341A) that was turned on andoff through a computer-based program.tation of a given CS 30 min postintubation, when

alcohol reaches peak concentrations in blood and During this second phase of the experiment thatbegan on the pups’ 12th postnatal day, pups in groupsbrain, facilitates aversive alcohol-mediated condi-

tioning (Hunt et al., 1990; Molina et al., 1989). It UP–P and P–P received an intragastric alcohol ad-ministration that yielded an alcohol dose equivalenthas been suggested previously that this procedure

shortens the functional delay between CS presenta- to the one employed in the first phase of the experi-ment (2.0 g/kg). The intubation procedure was per-tion and onset of aversive consequences of the toxic

state; conditioning in preweanling rats decreases formed 120 min after cannulation. Thirty minutesafter this alcohol administration, pups were individ-rapidly with increases in this delay (Hunt et al.,

1990). Texture conditioning in P–UP and P–P pups ually placed into holding chambers partially filledwith pine shavings where they received the sucrosewas performed during Postnatal Days 10 and 11 (one full

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infusion procedure for 10 min. Ingestion of the su-crose therefore occurred 30–40 min after receivingthe 2.0 g/kg alcohol dose. This ethanol–sucrose inter-val was the same as that employed during Phase 1 topair the texture CS with the peak period of alcohol’spostabsorptive effects (US). Pups in Group P–Ptherefore experienced both the texture CS (Phase 1,PDs 10 and 11) and the rewarding properties of thesucrose infusion (Phase 2, PD 12) after the sameinterval following alcohol administration.

Pups in groups UP–UP and P–UP were exposedto the sucrose infusion procedure 60 min after beingcannulated. The procedure was performed using thesame apparatus and temporal parameters for theremaining groups. One hour later, UP–UP and P–UPpups received the 2.0 g/kg alcohol dose.

All animals were tested for texture preferences 120min after receiving the 2.0 g/kg alcohol dose. Theapparatus used for texture preference testing was aclear Plexiglas rectangular box (28 × 10 × 13 cm).Half of the floor of this apparatus was made withthe soft side of the carpet used during first-order

FIG. 1. Time spent on the soft texture as a function of treat-conditioning and the remainder of the floor was the ment (UP, P–UP, or P–P) and time of assessment (first and secondrougher weave texture of the backside of a piece of minute). Group UP is composed of the collapsed values of groups

UP–UP and UP–P. Vertical lines represent standard errors ofthe same carpet, to minimize differences in the odorthe means.of the alternatives. Texture testing procedures were

conducted for a 2-min period. Subjects were placed onthe midline separating the soft and rough textures.Time spent on the soft texture was recorded for 1 ences for pups given UP during Phase 1, values

across these groups for each minute of the test weremin; at that time the pup was gently taken out ofthe chamber, repositioned in the midline surface of collapsed. The collapsed group will be referred to

as UP.the apparatus, and time spent on the soft surfacewas again recorded during the following 1 min. All Figure 1 shows texture preferences for each condi-

tion. A two-way mixed analysis of variance (ANOVA)experimenters were blind to the treatment conditionof each pup. The criterion for scoring an infant as was conducted on time spent over soft texture, with

Treatment as a between-groups factor (UP, P–UP, orbeing on the soft texture was at least three paws andthe head above that tactile cue (Miller et al., 1990). P–P) and Test Minute as a within-subjects factor

(first vs. second minute). ANOVA indicated a signifi-This strict criterion lowers baseline preferencescores, making it relatively difficult to demonstrate cant main effect of Test Minute along with a signifi-

cant interaction with Treatment, F(1,49) = 7.23, p <a conditioned aversion, but it ensures that a pup islocated over a given texture. .01 and F(2,49) = 4.66, p < .02, respectively. Post hoc

comparisons (Fisher’s least mean significant differ-ence with an α set at .05) were employed in order to

Results and Discussion further analyze these results. Subjects given the softtexture paired with alcohol intoxication and later

Groups given unpaired presentations of the soft subjected to explicitly unpaired presentations be-tween sucrose and alcohol (P–UP) spent significantlytexture and alcohol during Phase 1 (UP–UP and

UP–P) spent similar amounts of time on the soft side less time over the soft texture during the first minuteof the test than did UP rats (reflecting the acquiredof the apparatus during the first and second minutes

of the test (UP–UP: first minute = 28.62 ± 4.85 s, aversion to this texture) or P–P rats (reflecting thedevaluation effect). During the second minute of thesecond minute = 30.38 ± 5.57 s; UP–P: first minute =

32.00 ± 5.27 s, second minute = 33.00 ± 5.41 s; pre- test, however, all groups spent similar amounts oftime over the soft cue, indicating extinction as a con-sented are means ± SEMs). Because the subsequent

Phase 2 manipulations failed to affect texture prefer- sequence of nonreinforced exposure to CS. UP and full

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P–P groups did not differ during either minute, ex- experiment the conclusions derived from Experi-ment 1.hibiting similar preferences for the CS in accord with

the devaluation effect. In the present experiment, first-order conditioningprocedures with tactile–alcohol pairings were per-The pattern of results indicates that a conditioned

tactile aversion developed in P–UP rats as a function formed as in Experiment 1. The difference betweenthe present and the previous experiment arises inof pairing the soft texture with alcohol intoxication

during Phase 1. This conditioned aversion was regis- the procedures for Phase 2. In Experiment 2 halfof the animals were treated with alcohol and halftered only during the first minute of testing. Appar-

ently, nonreinforced experience with the tactile CS with water during Phase 2. Therefore animals wereexposed to explicitly paired or unpaired presenta-during this first minute was sufficient to extinguish

the conditioned aversion; during the second minute tions between sucrose and alcohol or sucrose andwater. This allowed us to equate sucrose-test delaysof the test these rats did not differ from controls given

unpaired CS and US presentations during Phase 1. across groups that differed in terms of the criticaltreatment (alcohol vs. water).Rat pups assigned to the P–P group were also ex-

posed to the pairing of soft texture (CS) and alcoholMethodduring Phase 1. Nevertheless, relative to pertinent

controls (UP group) these animals showed no evi-Subjectsdence of the conditioned aversion to the soft texture

acquired during Phase 1. The Phase 2 devaluation Eighty-four 10-day-old pups representative of 10treatment—pairing of the alcohol US with the appe- litters were employed. Genetic, housing, and rearingtitive reinforcer, sucrose—eliminated the condi- conditions were identical to those described in Exper-tioned tactile aversion. iment 1.

Before concluding that this pattern of results isindicative of a devaluation phenomenon, however, Experimental Designcertain procedural aspects of the experiment re-

Animals were quasi-randomly assigned to one ofquired further examination. In the devaluationeight groups defined as a function of three main fac-phase of this experiment (Phase 2) the delay betweentors under consideration: Associative Treatment dur-sucrose infusion and subsequent testing proceduresing the first-order conditioning procedures of Phasewas not equivalent across critical groups. For the1 [soft-texture CS paired (P) or unpaired (UP) withP–P group, sucrose was infused in closer temporalalcohol’s postabsorptive effects]; Drug Treatmentproximity (90 min) to the test situation than forduring Phase 2 [alcohol (EtOH) or tap water (W)];P–UP rats (180 min), to better achieve the unpairingand Type of association between drug and sucrosein the latter. Experiment 2 tested the reliability andinfusion, paired (P) or unpaired (UP). The quasi-generality of the results of Experiment 1 while exam-random distribution was constrained only by theining the possibility that sucrose interfered with sub-need to minimize the number of subjects from a givensequent expression of the texture aversion as a func-litter assigned to any group (no more than two pupstion of the delay existing between orosensoryfrom a particular litter, usually one of each gender,stimulation and texture testing procedures.were assigned to any group). The number of pupsassigned to each particular condition was as follows:

EXPERIMENT 2 UP–W–UP, n = 12; UP–W–P, n = 11; P–W–UP, n =11; P–W–P, n = 8; UP–EtOH–UP, n = 12; UP–For Experiment 1, pups given pairings of a softEtOH–P, n = 9; P–EtOH–UP, n = 9; P–EtOH–P,texture with the peak postabsorptive effects of intu-n = 12.bated ethanol acquired a conditioned aversion to that

texture. When this conditioning procedure was fol- Apparatus and Procedureslowed by the same postabsorptive effects of ethanolpaired with sucrose, an apparent devaluation effect Texture conditioning using the consequences of in-

tragastrically intubated alcohol as a US took placewas obtained: the acquired aversion for the soft tex-ture was decreased or eliminated. Before accepting during Postnatal Days 10 and 11. The apparatus and

experimental procedures employed in Experiment 1this straightforward interpretation of the results,however, we attempted to rule out alternative expla- were also used in the present experiment. In this

Phase, rats in the UP groups (UP–W–UP, UP–W–P,nations based on temporal factors that conceivablymight have arisen from our decision for handling UP–EtOH–UP, and UP–EtOH–P) received a 10-min

exposure to the soft CS carpet 1 h prior to the admin-the UP procedures, while testing in an independent full

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MOLINA ET AL.126

istration of a 2.0 g/kg alcohol dose. Paired groups(P–W–UP, P–W–P, P–EtOH–UP, and P–EtOH–P) re-ceived 10 min of CS exposure 30 min following intu-bation of the 2.0 g/kg alcohol dose.

Phase 2 was conducted during Postnatal Day 12.During this phase, half of the animals received intra-gastric administration of tap water (0.015 ml/g) whilethe remaining pups were administered an equivalentvolume of a 16.8% v/v alcohol solution that resultedin a 2.0 g/kg alcohol dose. Groups UP–W–UP, P–W–UP, UP–EtOH–UP, and P–EtOH–UP received an in-traoral infusion of sucrose 60 min prior to water oralcohol administration. Groups UP–W–P, P–W–P,UP–EtOH–P, and P–EtOH–P received the corres-ponding intragastric administration (water or EtOH)and 30 min later received a 10-min sucrose infusion.Intragastric administration, cannulation, sucrose in-fusion, and holding procedures replicated those de-scribed in Experiment 1.

After completion of Phase 2, all animals receiveda two-way locational test for texture preference. Test-ing procedures were performed 70 min after intra-gastric administrations of water or alcohol. Testswere conducted using an apparatus like that de-scribed in Experiment 1. Each test lasted 2 min andtime spent over the soft carpet was recorded duringeach minute.

Results and Discussion FIG. 2. Time spent on the soft texture as a function of treat-ment during the phase 1 (UP or P) and pairing procedures during

As was the case in Experiment 1, UP groups during phase 2 (UP or P). (B) The group that received water in phase 2,Phase 1 showed no differences in time spent over the UP–W, is composed of the collapsed values of groups UP–W–P

and UP–W–UP. (A) The group that received alcohol in phase 2,soft carpet whether pups were later given, duringUP–EtOH, is composed of the collapsed values of groups UP–Phase 2, intragastric administration of water (UP–EtOH–UP and UP–EtOH–P. Time over the soft texture was regis-W–UP: first minute = 27.5 ± 6.1 s, second minute =tered during the first and second minute of a two-way tactile

31.3 ± 5.8 and UP–W–P: first minute = 35.0 ± 5.3 locational test. Vertical lines represent standard errors of thes, second minute = 33.7 ± 6.6 s; mean ± SEM) or means.intragastric intubation of alcohol (UP–EtOH–UP:first minute = 27.8 ± 6.1 s, second minute = 28.3 ±4.8 s; UP–EtOH–P: first minute = 30.4 ± 4.9 s, second during the texture test (first and second minutes).

The ANOVA revealed a significant main effect ofminute = 35.8 ± 6.7 s; mean ± SEM). Therefore, val-ues corresponding to the UP–W–UP and UP–W–P Test Minute and a significant interaction between

Treatment and Test Minute, F(1,78) = 19.93, p < .001groups were collapsed for each minute of the test(Fig. 2A). The resulting collapsed group will be re- and F(2,78) = 4.36, p < .02, respectively. Fisher’s

post hoc comparisons (p < .05) were subsequentlyferred to as UP–W. Values corresponding to the UP–EtOH–UP and UP–EtOH–P groups were also col- performed in order to further analyze the Treatment

× Test Minute interaction. During Minute 1 P–W–UP,lapsed. This collapsed group will be referred to asUP–EtOH (Fig. 2B). P–W–P, and P–EtOH–UP groups exhibited signifi-

cant reductions in time spent over the soft carpetA three-way mixed ANOVA was conducted in orderto analyze time spent over the soft carpet. Between- relative to UP–W and UP–EtOH treatment condi-

tions, reflecting the acquired aversion to this texture.group factors were associative treatments used inPhase 1 and Phase 2 (UP, P–UP, and P–P) and the By the second minute of the test these three groups

showed a significant increase in time spent over thesubstance administered during Phase 2 (water orEtOH). The within-Ss factor was time of assessment soft carpet relative to the values attained during the full

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DEVALUATION OF ALCOHOL’S AVERSIVE PROPERTIES 127

first minute, indicating extinction. The fourth, deval- delay existing between sucrose infusion and test. Dif-ferences between these groups clearly argue againstuation, group—P–EtOH–P—also had paired tex-

ture–alcohol experiences during the conditioning the possibility that sucrose presented in close tempo-ral proximity to the test situation interferes with thephase, but this group exhibited no retention of Phase

1 conditioning; it did not differ from the first-order expression of the conditioned texture aversion underanalysis. This difference appears better interpretedconditioning unpaired control groups (UP–W and

UP–EtOH). These P–EtOH–P pups also were ob- through an associative mechanism leading to devalu-ation of alcohol’s US representation as a consequenceserved to spend significantly more time over the soft

carpet during the first minute than did P–W–P rats. of being paired with an appetitive reinforcer.Notice that these groups did not differ in terms ofthe delay between sucrose infusion and testing proce- EXPERIMENT 3dures. The sole difference between P–EtOH–P andP–W–P pups is that the former group experienced Experiments 1 and 2 strongly support the notionsucrose while intoxicated with alcohol and the latter that infants readily form an association between agroup experienced the appetitive reinforcer under a texture CS and aversive consequences arising fromnontoxic state. These results verify the devaluation an acute state of alcohol intoxication. Also supportedeffect obtained in Experiment 1 and indicate that was that alcohol–sucrose pairings following such tex-this effect is independent of the interval between ture–alcohol conditioning decreased the conditionedsucrose administration and test. aversion to the texture. As confirmed by the results of

The pattern of results obtained allows for several Experiment 2, the devaluation procedure employedconclusions. As in Experiment 1, infant rats acquired during Phase 2 (sucrose–alcohol intoxication) wasa conditioned texture aversion from two pairings of the factor responsible for the decrement in the aver-a specific texture and alcohol’s postabsorptive effects. sion conditioned during Phase 1. This experimentThe expression of the texture aversion was not state- allowed us to reject the hypothesis that the decre-dependent. P–EtOH–UP rats were tested 70 min ment in the conditioned response was due insteadafter receiving their Phase-2 2.0 g/kg alcohol dose to a procedural factor involving a differential delaywhile P–W–UP and P–W–P pups were tested after between sucrose infusion and the test for texturebeing exposed to only water in Phase 2, yet they preference.expressed equivalent aversions to the texture. Fur- It might still be argued, however, that the mecha-thermore, expression of the texture aversion was ob- nism leading to the devaluation effect during Phaseserved only during the first minute of the test. In 2 is not dependent upon the association of two stimulithe second minute of testing no differences remained, (sucrose ingestion and alcohol intoxication) with op-a phenomenon probably indicative of extinction due posite affective properties, but rather that the sa-to nonreinforced exposure to the CS during the first lience of ingesting the novel solution, sucrose, in as-minute of the test. sociation with alcohol intoxication during Phase 2

Of major importance for the present study was interfered somehow with retention of the memorythe evidence for a devaluation effect resulting from formed during Phase 1. If this was the case any sa-sucrose–alcohol pairings after pups had acquired the lient gustatory event, independent of its affectiveethanol-induced texture aversion; this procedure component, should lead to similar results as thoseeliminated the acquired aversion, replicating the re- obtained with sucrose. Therefore, we decided to em-sults of Experiment 1. In the present experiment, ploy a salient tastant other than sucrose duringwater-treated animals during Phase 2 exhibited a Phase 2 of Experiment 3. This stimulus consisted ofstrong conditioned aversion to the soft CS (groups a citric acid solution that has been shown to act asP–W–UP and P–W–P when compared to UP–W). Ap- an effective aversive unconditioned stimulus in 11-parently, a decrease in the texture aversion occurred day-old pups (Chotro et al., 1991).when alcohol was employed as a US in first-orderconditioning procedures and subsequently was Methodpaired with sucrose infusion (group P–EtOH–P), butnot when sucrose was either explicitly unpaired with Subjects and Experimental Designalcohol intoxication (P–EtOH–UP) or was not accom-panied by alcohol during Phase 2 (P–W–P and P–W– Forty-eight 10-day-old pups representative of five

litters were used. As in Experiment 1, pups wereUP). Groups P–EtOH–P and P–W–P differed interms of the drug administered during the devalua- quasi-randomly assigned to one of four groups (all

n’s = 11–13 pups) defined by specific manipulationstion procedure but were equivalent in terms of the full

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MOLINA ET AL.128

within the two phases of this study [Phase 1: the soft 41.54 ± 3.15 s, second minute = 35.85 ± 4.02 s; pre-sented values are means ± SEMs). It is clear thattexture was explicitly paired (P) or unpaired (UP)

with alcohol intoxication; Phase 2: alcohol intoxica- Phase 2 manipulations in these groups did not affecttexture preferences. Therefore, values across thesetion was either explicitly paired (P) or unpaired (UP)

with an intraoral infusion of citric acid]. Litter repre- groups for each minute of the test were collapsed.The collapsed group will be referred to as UP.sentation was equivalent across groups.

Figure 3 depicts the recorded texture scores. Dur-ing the first minute of evaluation, pups that experi-

Apparatus and Procedures enced the soft CS explicitly paired with the state ofintoxication (P–P and P–UP groups) spent less timeTexture conditioning in which alcohol intoxicationover this texture than did UP organisms. By theserved as a US was conducted during Postnatal Dayssecond minute of the test, P–P rats continued to ex-10 and 11. The apparatus and experimental proce-hibit strong soft rejection scores relative to controldures were similar to those employed in Experimentsorganisms (UP), but P–UP pups did not. These de-1 and 2. Briefly, unpaired groups (UP–UP and UP–P)scriptive observations were supported by a two-wayreceived a 10-min exposure to the soft side of the CSmixed ANOVA, in which Treatment (UP, P–P, or P–carpet 1 h prior to intragastric administration of aUP) represented the between-factor and Test Minute2.0 g/kg alcohol dose. Paired groups (P–P and P–UP)the within-factor (first vs second), and by Fisher’sexperienced 10 min of CS exposure 30 min followingpost hoc comparisons with an α level set at .05. Theadministration of the same alcohol dose.ANOVA revealed a significant main effect attribut-The second phase of this experiment took placeable to Treatment, F(2,45) = 7.37, p < .01. Post hocduring Postnatal Day 12. Groups P–P and UP–Ptests indicated that P–P and P–UP scores were sig-were again intubated with a 2 g/kg alcohol dose.nificantly lower than those recorded in UP subjectsThirty minutes later these subjects received a 10-during the first minute of evaluation. The condi-min citric acid infusion. Citric acid solution (0.04%tioned aversion to the texture was unaffected byw/v) was infused via oral cannulae that were individ-Phase 2 treatment at this point. During the secondually positioned in the subject’s cheek exactly as inminute, however, P–P scores were observed to be notExperiments 1 and 2. Pups in groups P–UP andonly significantly lower than those encountered inUP–UP were exposed to a similar citric acid infusion

procedure 1 h prior to the ig administration of 2 g/kg alcohol. The overall infusion rate of the citric acidsolution was equivalent to 5.5% of the preinfusionbody weight of each organism. This solution was in-fused using a pulsating rate (3 s on, 10 s off). For allanimals, oral cannulation procedures took place atleast 60 min prior to citric acid or alcohol administra-tion procedures. Citric acid infusions were regulatedthrough a Harvard Apparatus infusion pump (Model2265) and took place in individual holding chamberspartially filled with clean wood shavings.

All subjects were tested for texture preferences120 min after receiving the corresponding alcoholdose. The apparatus and procedures employed fortesting purposes replicated those used in Experi-ments 1 and 2.

Results and Discussion

Groups explicitly exposed to unpaired presenta-tions of the soft CS and alcohol during first-orderconditioning procedures (UP–UP and UP–P) spent

FIG. 3. Time spent on the soft texture as a function of treat-similar amounts of time on the soft side of the testingment (UP, P–UP, or P–P) and time of assessment (first and secondchamber during the first and second minute of the minute). Group UP is composed of the collapsed values of groups

evaluation (UP–UP: first minute = 39.45 ± 4.31 s, UP–UP and UP–P. Vertical lines represent standard errors ofthe means.second minute = 33.18 ± 6.8 s; UP–P: first minute = full

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DEVALUATION OF ALCOHOL’S AVERSIVE PROPERTIES 129

UP controls, but also significantly lower than those with alcohol’s postabsorptive affects, became aver-sive to the physiologically immature rat. The presentregistered in P–UP pups. At this latter point in test-

ing, Phase 2 treatment enhanced the texture study, coupled with the preliminary results reportedpreviously (Brasser et al., 1993), suggest that tactileaversion.

As seen in Experiments 1 and 2, pups that experi- cues also can be aversively conditioned in the devel-oping rat when paired with the state of acute alco-enced the soft texture paired with alcohol intoxica-

tion and that later had a similar state of intoxication hol intoxication.Acute alcohol intoxication was induced using in-explicitly unpaired with salient gustatory cues (P–

UP) showed reliable texture conditioned aversions tragastric administration of the drug. This proceduredoes not bypass exposure to alcohol’s orosensoryto the soft CS during the first minute of the test. By

the second minute the conditioned response seemed cues. As previously demonstrated, these cues are pro-cessed quite effectively by the infant animal severalto be extinguished. In turn, responsiveness to the soft

CS in P–P subjects appeared to be highly dependent minutes after intragastric administration (Chotro etal., 1991; Dominguez, Bocco, Chotro, Spear, & Mol-upon the nature of the gustatory cue paired with the

state of acute alcohol intoxication during Phase 2. ina, in press; Molina & Chotro, 1989a,b; Molina et al.,1989). Direct elimination of the drug via respirationIn the first two experiments, sucrose infusions paired

with alcohol intoxication were found to devalue tex- and/or salivation and hematogenic stimulation ofchemosensory receptors seem to represent theture conditioned aversions. In the present experi-

ment, citric acid infusions paired with the state of sources of orosensory experience with alcohol-de-rived cues during the state of intoxication. Accordingintoxication did not affect the initial magnitude of

the conditioned response (first minute of the test) to a previous study, infantile perception of alcohol’sorosensory attributes reaches a peak level 30 to 60accrued through prior texture–alcohol pairings. Not

only did it fail to affect the expression of the aversion min after intragastric administration of alcohol (Mol-ina & Chotro, 1989a). In the present experimentsduring the first minute of the test, but it also seemed

to augment resistance to extinction of the aversion the tactile CS employed during the first-order condi-tioning procedures was presented 30–40 min afterconditioned during Phase 1. By the second minute

of the test, P–P animals in the present experiment intragastric administration of ethanol. Therefore, itis possible that infants experienced a compound CSstill evidenced robust conditioned texture aversions

when compared to appropriate controls. (alcohol’s orosensory properties plus soft texture)rather than a single element CS (soft texture) pairedwith the US (alcohol intoxication). Infants tend toGENERAL DISCUSSIONintegrate co-occurring events and exhibit greaterconditioning to a given sensory stimulus that wasThe results of this study demonstrate: (1) Infant

rats can acquire an association between a salient originally configured with other cues than when thestimulus was employed as a single CS during acquisi-tactile cue (texture) and alcohol’s postabsorptive ef-

fects, leading to the expression of a conditioned tex- tion of the conditioned responses (Kucharski &Spear, 1985; Molina, Hoffmann, Serwatka, & Spear,ture aversion (Experiments 1–3); (2) The memory of

this aversion is malleable and can be eliminated or 1991; Spear, Kraemer, Molina, & Smoller, 1988;Spear & Kucharski, 1984).reduced by devaluing the US with sucrose intraoral

infusions after conditioning (Experiments 1 and 2); These considerations appear relevant when ana-lyzing potential mechanisms responsible for the cur-(3) The reduction in the conditioned texture aversion

resulting from Phase 2 pairings of alcohol and su- rent devaluation effect. During the devaluationphase, animals experienced sucrose 30–40 min aftercrose was not observed when employing an alterna-

tive salient tastant with aversive US properties (cit- being intubated with alcohol. Sucrose presentationat this time apparently competes with alcohol’s aver-ric acid; Experiment 3).

Ethanol intoxication has been shown to act as an sive US capabilities, so that the pup becomes appeti-tively conditioned to alcohol’s orosensory cues per-aversive reinforcer during early ontogeny. Yet the

previous literature addressing ethanol’s US capabili- ceived during the state of intoxication (Hunt et al.,1990; Molina & Chotro, 1989a). It is possible thatties in infant organisms is based on conditioning pro-

cedures in which only chemosensory stimuli were the present devaluation effect is due to an a betweenthe texture and sucrose, mediated through the stimu-employed as CSs. Sucrose (Hunt et al., 1990), milk

(Hunt, Kraebel, Rabine, Spear, & Spear, 1993), and lus consequences of alcohol—orosensory cues andpharmacological consequences—that were commonalcohol odor and/or taste (Molina & Chotro, 1989a;

Molina et al., 1989; Molina et al., 1984), when paired to both phases of the experiment and so paired with full

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MOLINA ET AL.130

each of the texture and sucrose (Spear et al., 1988). ceived the soft CS texture paired with alcohol fol-lowed by unpaired presentations of sucrose or citricThe alternative, more conventional interpretation

of the present results is based on the notion that acid and alcohol (groups P–UP), later exhibitedstrong rejection scores of the soft texture. These aver-infants acquire memories that can be modified by

experimental manipulation of their US representa- sions rapidly seemed to extinguish. By the secondminute of the test, texture scores of P–UP groupstion. It has been previously shown (Kraemer et al.,

1992) that 10-day-old pups, given pairings of an ap- were very similar to those of unpaired controls. Mostof the locational tests employed for the assessmentpetitive US (heat) and an aversive US (footshock),

reflect devaluation in terms of reduced preference to of early visual (e.g., Miller & Spear, 1989), olfactory(e.g., Kraemer et al., 1992; Kucharski & Spear, 1984;an olfactory CS previously paired with the appetitive

US (heat). In this alternative perspective, after pups Arnold & Spear, 1993), and tactile conditioned re-sponses (e.g., Miller et al., 1990), have a short dura-in the present experiments acquired an aversion to

the texture as a consequence of its pairing with alco- tion (1 to 3 min). It has been observed that a briefodor locational test (overall duration: 3 min; timehol US properties, the pup’s representation of these

properties was changed (devalued) during Phase 2 spent over CS+: 80–110 s) is sufficient to promoteextinction of an olfactory conditioned aversion estab-by pairing the state of alcohol intoxication with an

appetitive sucrose infusion. The texture CS, accord- lished via odor–LiCl pairings during Postnatal Day8 (Miller et al., 1990). Also, it is quite possible thatingly, elicited conditioned aversion of a lesser magni-

tude than observed in controls given unpaired pre- extinction would take longer if Phase 2 was not exe-cuted. Reexposure to the CS, in this case soft texturesentations.

The results of Experiment 3 showed that the de- during testing, while the original training memoryis active could help learning of the new contingencycreased texture aversion in P–P groups induced by

Phase 2 devaluation (Experiments 1 and 2) could not (extinction) (Arnold & Spear, 1993). Indeed, Phase 2implies reexposure to alcohol which was employedbe obtained if citric acid rather than sucrose was

paired with alcohol intoxication during Phase 2. On as a US in Phase 1. A prior-cuing treatment such asUS reexposure is highly effective in terms of promot-the contrary, citric acid paired with alcohol intoxica-

tion appeared to strengthen texture conditioned ing a reactivation effect (Miller, Jagielo, & Spear,1991).aversions in terms of increased resistance to extinc-

tion. As previously demonstrated, citric acid solu- The present results confirm and extend prior ob-servations of the effectiveness of alcohol’s primarytions act as aversive unconditioned stimuli in pre-

weanling organisms while sucrose solutions act as aversive US properties during early developmentand suggest that these properties may become associ-appetitive reinforcers (Chotro et al., 1991; Molina &

Chotro, 1989a). This suggests that the affective na- ated with tactile as well as chemosensory events.Both kinds of events are known to play a major roleture of the unconditioned stimulus paired with alco-

hol intoxication during Phase 2 was the critical factor in the modulation of early suckling behavior (Hofer,1987). Recent studies suggest that infants can bein modulation of the magnitude of the previously

acquired texture aversion. exposed to alcohol’s toxic properties as a result ofbreast feeding experiences comprising milk contami-Variation in the intensity of the US during postcon-

ditioning revaluation procedures is known to affect nated with this drug (Mennella & Beauchamp, 1991).For maternal–infantile interactions in such a nurs-the magnitude of the conditioned response (Dela-

meter & LoLordo, 1991). Generally, postconditioning ing situation, the role of tactile and chemosensorycues paired with alcohol’s toxic effects remains toexposure to a less intense version of the US leads to

a weakened conditioned response while inflation of be investigated.Finally, the present results attest to the plasticitythe conditioned response tends to occur when post-

conditioning exposure is conducted with a more in- of the infant rat in terms of the modification of priorconditioning and suggest that the biphasic hedonictense version of the US. In the experimental circum-

stances of Experiment 3, perceived intensity of effects of alcohol might profitably be analyzed experi-mentally through elimination of alcohol’s aversivealcohol intoxication as a US during Phase 2 could

increase due to contingent presentation of an addi- US properties by devaluation procedures. As recentlydemonstrated, alcohol’s appetitive and aversive ef-tional aversive US such as citric acid. Prior research

indicates that a compound US involving two qualita- fects coexist within the state of intoxication (Ris-singer & Cunningham, 1992). Temporal overlap oftively different aversive stimuli can lead to enhanced

aversive learning (Lasiter & Braun, 1981). these appetitive and aversive effects of differentialmagnitude present an obstacle in the analysis of alco-Across the different experiments, groups that re- full

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order appetitive conditioning. Journal of Experimental Psy-hol’s US effects. To our knowledge the derivation ofchology: Animal Behavior Process, 1, 355–363.appetitive properties from the state of intoxication

Hunt, P. S., Kraebel, K. S., Rabine, H., Spear, L. P., & Spear,has not been demonstrated in preweanling organ-N. E. (1993). Enhanced ethanol intake in preweanling ratsisms. Conditioned aversions have seemed to repre- following exposure to ethanol in a nursing context. Develop-

sent the prevailing consequence at this age when mental Psychobiology, 26, 133–153.alcohol acts as the US. A devaluation procedure pro- Hunt, P. S., Molina, J. C., Spear, L. P., & Spear, N. E. (1990).vides an experimental tool that might permit more Ethanol-mediated taste aversions and state-dependency in

preweanling (16-day-old) rats. Behavioral and Neural Biology,effective control over the aversive component of etha-54, 300–322.nol’s consequences and allow the expression and

Kraemer, P. J., Hoffmann, H., Randall, C. K., & Spear, N. E. (1992).analysis of its appetitive consequences.Devaluation of Pavlovian conditioning in the 10-day-old rat.Animal Learning and Behavior, 20, 219–222.

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