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Contents lists available at ScienceDirect

Behavioural Processes

jo ur nal homep ag e: www.elsev ier .com/ locate /behavproc

ntertrial intervals and contextual conditioning in appetitiveavlovian learning: Effects over the ABA renewal paradigm

odrigo Carranza-Jassoa, Gonzalo P. Urcelayb, Javier Nietoa, Livia Sánchez-Carrascoa,∗

División de Investigación y Posgrado, Facultad de Psicología, Universidad Nacional Autónoma de México, MexicoDepartment of Psychology, University of Cambridge, United Kingdom

r t i c l e i n f o

rticle history:eceived 10 February 2014eceived in revised form 9 July 2014ccepted 27 July 2014vailable online xxx

eywords:ontext

ntertrial intervalatenewal

a b s t r a c t

Three experiments using rats in an appetitive conditioning procedure analyzed the effect of short and long(50 s vs. 1440 s) intertrial intervals (ITI) over the acquisition of conditioned stimulus (CS), context (Ctxt),and unconditioned stimulus (US) associations, as well as the effect on the extinction and renewal of theconditioned response to the CS. Experiment 1 revealed more contextual conditioned responses in groupstrained with the short ITIs, however the renewal effect was not observed during test phase with eitherITI condition. When subjects were pre-exposed to the contexts before the acquisition phase (Experiment2) renewal of the conditioned response (CR) was only observed in long ITI group. However, when theacquisition context was extinguished (Experiment 3) the renewal effect observed in the Experiment 2was weakened. In all three experiments subjects showed a similar number of responses to the tonepredicting food, however they showed a clear contextual conditioning effect only for the groups trainedwith short ITIs. It is noteworthy that the acquisition context showed high levels of the CR in the renewal

test only for groups trained with short ITIs (Experiment 2) but these responses were absent if additionalcontextual extinction was imposed before such test (Experiment 3). In general, all groups showed similaracquisition curves for the CS but only Short groups had an increase in the CR during the pre-CS. Also,context conditioning does not interfere with the conditioning of the CS and context pre-exposure priorto acquisition is essential in order to observe the renewal effect when long ITIs are used.

© 2014 Published by Elsevier B.V.

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. Introduction

Nowadays there is a growing interest in understanding how con-extual stimuli influence behavior (e.g. Urcelay and Miller, 2014;olland and Bouton, 1999; Maren et al., 2013), since it has beenbserved that these stimuli plays a key role in associative learn-ng. The intertrial interval (hereafter, ITI) has been one of the mosttudied variables when contextual learning is analyzed.

The importance of the ITI length over the development of theavlovian conditioning has been pointed out by several researchersBarela, 1999; Gibbon and Balsam, 1981; Miller and Matzel, 1988;

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

escorla and Wagner, 1972; Wagner, 1981). For example, Rescorland Wagner (1972) suggested that the ITI length plays an impor-ant role in the strength of the conditioned stimulus (CS) and

∗ Corresponding author at: Cognitive and Neuronal Mechanisms of Learning Lab-ratory, B-021, Edificio B, Facultad de Psicología, Universidad Nacional Autónomae México, Av. Universidad 3004, Col. Copilco-Universidad, 04510 Delegaciónoyoacán, DF, Mexico. Tel.: +52 55 56222242.

E-mail addresses: livia@unam.mx, lyvia.sanchez@hotmail.comL. Sánchez-Carrasco).

ttp://dx.doi.org/10.1016/j.beproc.2014.07.014376-6357/© 2014 Published by Elsevier B.V.

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the unconditioned stimulus (US) associations, as well as the Con-text–US associations. These authors propose that during the condi-tioning trials, two associations are strengthened: one between theCS and the US, and other between the Context and the US, becauseboth stimulus (i.e. Context and CS) are present when the US is deliv-ered at the end of the trial. However, during the ITI, Context–USassociations are weakened (i.e. extinction) because the context isthe only stimulus present during these intervals, and no reinforcersare presented during the ITI. Accordingly, short ITI lengths result inmore contextual conditioning, while long ITI lengths result in lesscontextual conditioning (e.g. Terrace et al., 1975). Additionally, it isexpected that the associative strength of the CS be affected by thisContext–US association, thus with short ITIs there is more com-petition between the CS and the Context for associative strength,and with long ITIs the CS acquire the associative strength easilybecause context’s associative strength is extinguished during theseintervals. For example, Rescorla and Durlach (1987) showed in a

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

within-subjects autoshaping experiment with pigeons as subjects,that ITIs produced greater conditioning to a CS trained with longITI, as well as, a context having short ITIs showed greater ability topromote responses to stimuli trained in any other context.

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Sunsay and Bouton (2008) conducted a similar experiment withats trained in an appetitive conditioning procedure. In their Exper-ment 1, they exposed eight groups of rats during 16 acquisitionessions to four daily trials where a 30 s tone was paired with foodellets; each group was conditioned using a different ITI lengthi.e. 60, 120, 180, 240, 480, 960, 1440 and 1920 s). The food-cupntries during the CS and during the 30 s before the CS (i.e. pre-CSr pre-period) were registered as CRs to the CS and to the con-ext, respectively. Acquisition showed a decreasing tendency inhe amount of food-cup entries during the pre-CS as the ITI lengthncreased, but the CR to the tone was relatively constant across allhe different ITI lengths. The authors concluded that the decreasen the response level in the pre-CS period reflects the decrease ofhe Context–US associative strength. These results were consistentith the Rescorla and Wagner (1972) model’s prediction regarding

he extinction of the Context–US association during the ITI, thuss the ITI length increases, more contextual extinction should bebserved. In conclusion, the length of the intertrial interval affectshe strength of the CS and context conditioning. Most findings sug-est that long intertrial intervals results in high conditioning tohe CS, and short intertrial intervals produce high contextual con-itioning. This evidence comes to relevance in several contextualhenomena, particularly in the ABA context renewal paradigm.

The context renewal effect is usually observed in proceduresrranged in three phases: Acquisition, Extinction and Test. Particu-arly, in the ABA renewal design the acquisition phase is conductedn Context A, the extinction phase occurs in Context B and theest phase keeps the same conditions of extinction but the sub-ects return to the acquisition context (Bouton and Peck, 1989;outon and Ricker, 1994; Brooks and Bouton, 1994). Addition-lly, contextual renewal has been observed when the acquisitionnd extinction contexts are the same, while test context is differ-nt (i.e. AAB renewal), as well as when the contexts used in eachhase are different (i.e. ABC renewal). To account for these obser-ations, Bouton (1993) suggested that the context renewal effect isbserved when extinction treatment is given in a different contextrom that used during the extinction phase. Thus, context renewals expected when extinction and test contexts differed. Also, it isssumed from Bouton’s explanation of the renewal effect that theevel of response recovery should be similar in all designs, how-ver findings using very different preparations (e.g. instrumentalonditioning, fear conditioning) have failed to supports this pre-iction (e.g. Nakajima et al., 2000; Thomas et al., 2003), in fact itas been observed higher levels of context renewal when the ABAenewal design was used. In agreement some authors have sug-ested that some contextual conditioning could be observed duringhe acquisition (Lovibond et al., 1984; c.f. Bouton and King, 1983).or example, some experiments have showed a reduction in theevel of response when acquisition context is changed after theonditioned response has been acquired. Additionally it has beenbserved that the context and the conditioned stimulus competen order to acquire associative strength and this could be affected,mong several factors, by the length of the intertrial interval.

Since the ABA design is the only renewal design that uses thecquisition context in the test phase, it is reasonable to assesshether a higher response recovery in this design could beroduced by an interaction between the mechanism proposedy Bouton (i.e. context change between extinction and test) andhe associative strength of the acquisition context. Bouton anding (1983) tested this possibility in four conditioned suppressionxperiments. In these experiments, they found that the ABAenewal effect does not depend on contextual conditioning of the

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

est context but still they were able to find contextual conditioningf the acquisition context and they were not able to determinef such contextual conditioning played a role in the renewalffect. In order to test these assumptions in a pavlovian appetitive

PRESS Processes xxx (2014) xxx–xxx

procedure, we designed three experiments to assess if the trainingITI length may affect contextual conditioning, and if this contextualconditioning may increase ABA renewal. Particularly, we assessedif subjects trained with short ITI lengths show a higher renewaleffect that those trained with long ITIs.

2. Experiment 1

In the first experiment, four groups of rats were trained in anappetitive conditioning procedure where a 30 s tone was pairedwith food. All groups were trained during six sessions in Con-text A, in two groups (i.e. ABA Short, AAA Short), trials werespaced by short ITIs (i.e. 50 s), whereas in the other two groups(i.e. ABA Long, AAA Long) long ITIs (i.e. 1440 s) were used. Thenall groups underwent extinction. AAA Short and AAA Long groupsreceived extinction trials in Context A, while ABA Short and ABALong received extinction in Context B. Finally, all subjects weretested in the context where training occurred. During the last twophases of the experiment, all groups were extinguished and testedusing an intermediate ITI length (i.e. 275 s). This design allowedus to assess the effect of contextual conditioning in acquisition,extinction and contextual renewal. Since AAA Short and ABA Shortgroups were trained with short ITI lengths we expected to observehigh levels of contextual conditioning, while in AAA Long and ABALong low levels of contextual conditioning were anticipated (e.g.Denniston et al., 2003; Mustaca et al., 1991; Rescorla and Durlach,1987; Sunsay and Bouton, 2008; Urcelay and Miller, 2010). Addi-tionally, in this experiment we omitted the pre-exposure phasedescribed in most appetitive classical conditioning renewal exper-iments (Bouton et al., 1993; Bouton and Peck, 1989; Brooks andBouton, 1994; Ricker and Bouton, 1996), in order to avoid a pos-sible interaction between latent inhibition of the context and ITIlength, as it has been observed (at least in aversive conditioningprocedures) that context pre-exposure results in latent inhibitionto the context (Cole et al., 1996; Urcelay and Miller, 2010).

2.1. Method

2.1.1. SubjectsThe subjects were 48 experimental naïve Wistar rats (6 male

and 6 female per group) bred at the Psychology school vivarium(Universidad Nacional Autónoma de México). They were approxi-mately 90 days old and weighing 200–350 g at the beginning of theexperiment and were housed individually in standard cages, in acolony room. The experiment was conducted on consecutive daysduring the light portion of the day. The rats were food deprivedand maintained at 83% of their free-feeding weights throughoutthe experiment, they also had free access to water on their indi-vidual Plexiglas home cages and at the end of every session theyreceived complementary food to keep them on their deprivationgoal weight.

2.1.2. ApparatusExperimental sessions were conducted in six MED Associates®

conditioning chambers measuring 20.8 × 21 × 28.2 cm (h × l × w).Each chamber consisted of a front and a rear stainless steel panel,while the superior panel and sidewalls were made of clear acrylicsheets. The floor of all chambers consisted on 16 tubular stainlesssteel bars, of 0.5 cm diameter, separated by a 1.5 cm center-to-center gap and which were located parallel to the front panel. Inthe center of the front panel and 1 cm above the floor, there waslocated a 5 cm × 5 cm quadrangular opening and inside of it a food-

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

cup was located. Behind the front panel was a pellet dispenser,which delivered 45 mg Bio-Serv Dustless Precision Pellets®, rodentgrain based diet (Bio-Serv, Frenchtown, NJ). The US was the presen-tation of two 45 mg Bio-Serv precision pellets delivered 0.2 s apart

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Table 1Design of Experiment 1.a

Groups Acquisition Extinction Test

ABA Short A: T+ ITI: 50 s B: T− ITI: 275 s A: T− ITI: 275 sABA Long A: T+ ITI: 1440 s B: T− ITI: 275 s A: T− ITI: 275 sAAA Short A: T+ ITI: 50 s A: T− ITI: 275 s A: T− ITI: 275 sAAA Long A: T+ ITI: 1440 s A: T− ITI: 275 s A: T− ITI: 275 s

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a Note: The A and B characters designate the context where the correspondinghase was conducted, while T stands for the presentation of the tone either inresence (+) or in absence (−) of the US.

rom each other, at the termination of the CS. In all experimentalessions each trial begun with the onset of the CS and finished withhe offset of the CS, which was concurrent with the delivery of theS. Thus the ITI was defined as the period between the offset of theS and the onset of the next CS. Above the food-cup was a speakerhat produced a 2900 Hz tone with duration of 30 s, which was useds CS. On the center of the rear panel and 2 cm below the superioranel was a 28 V DC light bulb, which provided general illuminationo the conditioning chamber.

All the chambers were inside sound attenuating boxes equippedith a 28 V ventilation fan, which also provided background whiteoise. Experimental sessions and data recording were conductedhrough an interface (MED Associates® Mod. SG-502) that con-rolled the chambers, and that was connected to a Pentium III PCith the MED-PC IV software installed on it. As CR, the interrup-

ions to an infrared photocell located on the food-cup opening wereecorded, as well as stimuli presence and their corresponding timesf occurrence were registered.

.1.3. Contextual stimuliThe six conditioning chambers formed a matrix of three rows

y two columns. In order to conduct the experimental sessions,he conditioning chambers were adapted to provide two differentnd distinctive contexts. These contexts differed on their olfactory,actile and location features (Thomas et al., 2003). Both contextsere counterbalanced for all subjects.

The boxes in the left column (Lavender Sandpaper Context)ad the chamber floor covered with number 80 wood sandpaperFandeli® F Sandpaper) and a container with 15 ml of lavender liq-id cleaner FABULOSO Fresh Lavender® (Colgate-Palmolive, S.A.e C.V., D.F., Mexico) was placed under the food-cup. On thether hand, the boxes in the right column (Vinegar Bars Context)ept their stainless steel bars flooring and a container with 15 mlf acetic acid (Cane Alcohol’s White Vinegar Clemente Jacques®,ABORMEX S.A. de C.V., D.F., Mexico) was also placed under theood-cup. The olfactory and tactile stimuli used in each contextere replaced every two days.

.1.4. ProcedureThe experimental sessions were conducted on consecutive days

nd at the same time of the day. The experiment consisted of threehases: acquisition, extinction and test (see Table 1).

The acquisition phase was conducted on Context A and wasffective for six sessions. On each session four appetitive condition-ng trials took place. Every trial consisted of a tone presentation for0 s, followed by the delivery of two food pellets. During this phasehe mean ITI length for the Short groups was of 50 s (the ITI valuesanged from 35 to 68 s), while the mean ITI length for Long groupsas of 1440 s (the ITI values ranged from 1100 to 1900 s).

The extinction phase consisted of six sessions and was con-ucted on a different context from the acquisition context (Context

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

) for the “ABA” groups, while for groups AAA this phase was con-ucted in the same context used for acquisition (Context A). Thus,he AAA groups experienced the extinction phase in an alreadyamiliar context, while the ABA groups experienced extinction in

PRESS Processes xxx (2014) xxx–xxx 3

a novel context. In this phase all groups were exposed to fourtrials per session, where they experienced presentations of thetone alone, using a mean ITI length of 275 s (the ITI values rangedfrom 200 to 350 s). This intermediate interval was calculated usingthe geometric mean of the intervals employed during acquisition,trying to eliminate differential biases due to possible extinctioninterval similarity with the acquisition interval (vid. Gallistel andGibbon, 2000). Finally, on the test phase, the extinction contingen-cies remained in effect and consisted of one session. All groupsexperienced this phase in Context A.

2.1.5. Data analysisResponse during both the CS and the 30 s period before the CS

(pre-CS), as well as the elevation scores, were used as dependentvariables. Elevation scores are usually used in the literature to bet-ter reflect the conditioned control of the CS over the CR (Bouton andRicker, 1994; Brooks and Bouton, 1994). Following this reasoning,we assume that responses during the CS reflect the CRs elicited bythe tone’s associative strength alone, while the responses duringthe pre-CS reflect the CRs produced by the context’s associativestrength and, thus, the elevation scores represent a measurementof which stimuli (i.e. CS vs. Context) has better control over theCR. If the elevation score has near zero values or lower, then theCS has a weak control over the CR, but if the elevation score val-ues are higher than zero, then the CS has a stronger control overthe CR. These elevation scores are obtained by subtracting the pre-CS responses from the CS responses. The individual data of eachsubject were analyzed in order to find response levels that werenumerically distant from the rest of the data (i.e., outliers). Thismeasure was taken because after an overview inspection of thedata, high levels of variability seemed to be present. Particularly,this variability seemed to originate in data from particular sub-jects that behaved in an extreme fashion and such behavior didnot follow the contingencies established in each phase. In orderto determine if such variability could be due to the presence ofoutliers and extremes, the experimental data were analyzed inorder to search for such anomalous scores. Although there is a wideamount of literature regarding ways to determine whether a par-ticular datum is an outlier or not, there is no clear agreement ofthe criteria to keep or eliminate such outlier or extreme datum.Thus, we considered an outlier as such, if this individual data fulfillsany of the following criteria: (a) data value > UBV + o.c. × (UBV-LBV),or (b) data value < LBV − o.c. × (UBV-LBV); where UBV stands forthe upper value of the box (e.g. median + the 75th percentile) ina box plot of such data, LBV stands for the lower value of suchbox plot (e.g. median − the 25th percentile) and o.c. is an outliercoefficient (e.g. regularly set by default and used in this anal-ysis in a value of 1.5). In the other hand, a datum value wasconsidered an extreme, if such individual data fulfills any of thefollowing criteria: (a) data value > UBV + 2 × o.c. × (UBV-LBV), orb) data value < LBV − 2 × o.c. × (UBV-LBV). Therefore, we analyzedboth the CS and pre-CS responses for each session of the experi-ment by group through a box plot graph (Osborne and Overbay,2004; Barnett and Lewis, 1994). When a subject’s responses dataset presented outliers in the 25% or more of the data values of allexperimental sessions, its whole data set (i.e. CS, pre-CS and ele-vation scores) was excluded from the data analysis. The responsesof all subjects in each group were averaged for session unless it isstated otherwise and the rejection criteria for all statistical analysiswas set at ̨ = .05.

2.2. Results and discussion

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

2.2.1. AcquisitionAccording to the outlier’s exclusion criteria only one subject in

the AAA Long group was eliminated of the data analysis. Since the

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Fig. 1. Experiment 1: mean responses during the CS, the pre-CS and the ele

nly difference among groups during the acquisition phase was theTI length used, responses were collapsed as Short and Long (panel

of Fig. 1). The mean food-cup entries to the CS increased simi-

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

arly across sessions for Long and Short group. However responsesuring the pre-CS increased only for the Short group. The mean oflevation scores in the Long group increased throughout the phasehile the elevation scores for the Short group remained below

able 2tatistical analysis of Experiment 1.a

Phase Effect

AcquisitionITI Length

Session

ITI Length × Session

ExtinctionITI Length

Extinction Context

Session

ITI Length × Extinction Context

ITI Length × Session

Extinction Context × Session

ITI Length × Extinction Context × Session

TestITI Length

Extinction Context

ITI Length × Extinction Context

a Note: This table shows the F scores of main effects and interactions during acquisition* F scores with p values lower than 0.05.

scores obtained during (A) acquisition, (B) extinction and (C) renewal test.

zero during the whole phase. The means of food-cup entries bothto the CS and during the pre-CS, as well as the elevation scores,were analyzed with a mixed 2 (ITI Length) × 6 (Session) ANOVA (see

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

Table 2). This analysis of the mean of responses to the CS revealeda reliable main effect for the Session factor. The pre-CS responsesshowed a main effect for the Session and ITI Length factors. Finally,the elevation scores revealed a reliable main effect for the Session

F scores

CS Pre-CS Elevation score

0.8261 163.9952* 123.2311*

18.7607* 2.2997* 11.8805*

2.1644 1.4163 5.3728*

6.2763* 19.9973* 2.711237.3414* 0.1244 8.50434*

15.7551* 10.2091* 1.958830.0774 11.9702* 11.54885*

0.6393 0.9594 1.784161.7286 0.9359 2.83390*

0.7143 3.3460* 2.20959

0.03598 4.04385 3.1019172.21476 0.06962 1.7264130.43950 0.01707 0.330733

, extinction and test of Experiment 1.

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nd ITI Length factors as well as a significant interaction betweenhem.

The differences observed between groups during the pre-CSeriod are in agreement with the Rescorla and Wagner (1972)roposal, which states that during acquisition phase Context–USssociations are formed as well as CS–US associations, so that bothhe Context and the CS acquire associative strength. Accordingly,hen long ITIs are used during acquisition, the context is present

or a long period of time (i.e. 1440 s) with no presentation of the US,o these Context–no US “trials” may function as extinction for theontext’s associative strength, hence a low level of responding isbserved in Long group. Conversely, when short ITIs were used (i.e.0 s), it is unlikely that context extinction can be observed; there-ore during the pre-CS high levels of responding were present inhe short groups.

.2.2. ExtinctionPanel B of Fig. 1 shows the decrease in responding of the

our groups during the extinction phase. We used a mixed 2 (ITIength) × 2 (Extinction Context) × 6 (Session) ANOVA to analyzehe responses of this phase (Table 2), The CS scores showed a reli-ble effect for the ITI Length, Extinction Context and Session factors,lthough neither of the interactions among these factors was sig-ificant. The significant difference observed with the main effectf ITI Length showed that the mean of responses to the CS wasigher during this phase for Short groups than for Long groups.dditionally, the global mean of responses in the whole phase for

he groups extinguished in the acquisition context were higher thanhose extinguished in a new context. Finally, the significant differ-nce of the main factor session confirms the decreasing in the meanf responses through the extinction phase.

The pre-CS responses revealed a reliable effect for the ITI Lengthnd Session factors, as well as the ITI Length × Extinction Con-ext and the ITI Length × Extinction Context × Session interaction.hese results suggest that responses to the pre-CS period decreasedifferentially between groups depending on the context. Thus, sub-

ects that received acquisition and extinction in the same contexti.e. AAA groups) showed a differential level of responses duringhe pre-CS period, that is long ITI length group responded lessuring the pre-CS period than short ITI group, as revealed by alanned comparison, F(1, 258) = 30.77, p < 0.05. On the other hand,roups extinguished in a different context (i.e. ABA groups) showedquivalent levels of pre-CS responses across the extinction ses-ions. Acquisition and extinction results would jointly suggest thathen short ITIs were used during training, high contextual con-itioning took place, as evidenced by the high level of food-cuppproach responses registered during the pre-CS period. However,ow levels of response were observed in long ITIs groups, suggest-ng an effect of contextual extinction during the long ITIs employeduring the acquisition phase. When CS extinction was conducted

n a new context (i.e. ABA groups) the pre-CS responses of theBA Long group, at the beginning of the extinction phase, wereigher than those observed in AAA Long and decreased across theessions. It is possible suggest that this difference between AAAnd ABA Long groups could be brought by the presentation of aamiliar object, in this case, the food-cup, in a novel context. Forxample, recently Balderas et al. (2008) showed that rats placedn a novel or a familiar context with a familiar object, explore thebject more in the novel context than in the familiar one (see also,ampese and Delamater, 2013 for similar results). Thus, the nov-lty of Context B for ABA Long group, could produce that subjectsecognized the food-cup, but not its relation with the novel con-

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

ext.The elevation scores did not show changes in Short groups,

ut a steeply decline in the elevation score of ABA Long group. Aixed ANOVA analysis (see Table 2) yielded a main effect of the

PRESS Processes xxx (2014) xxx–xxx 5

Extinction Context factor, as well as ITI Length × Extinction Con-text and Extinction Context × Session interactions. These findingscould suggest some context dependency of acquisition only in ABALong group. Similar findings have been interpreted as showing thatcontextual cues can modulate CS–US associations, providing infor-mation that a specific CS–US relationship is effective, or helping thesubjects to retrieve information about the consequences of the CS(see Preston et al., 1986; Bonardi et al., 1990; Balaz et al., 1981a).Lovibond et al. (1984) have provided two alternative proposals toexplain the change in the response level when CS is tested in acontext different from that used during the conditioning. One pos-sibility is that the change of context modifies the way in which theCS is perceived, thus producing generalization decrement. The sec-ond explanation is that the magnitude of the CR is related to thecontribution of other associations (e.g. Context–US) that are debil-itated when the CS is presented in a novel context. As could beobserved in Fig. 1 panel B the elevation scores of AAA Short, ABAShort and ABA Long groups decreased during the first extinctionsessions, while the level of responses for AAA Long group was simi-lar to that observed in the last acquisition session. Since, the contextchange seems to interact with the ITI length used during the acqui-sition phase, our findings could not be explained as a generalizationdecrement.

2.2.3. Renewal testThe scores of the test phase are depicted in panel C of Fig. 1. A fac-

torial 2 (ITI Length) × 2 (Extinction Context) ANOVA conducted forthe responses to the CS, the pre-CS and the elevation scores revealedneither reliable effects nor interactions for any of the response mea-surements (see Table 2). In conclusion, these results do not replicatethe ABA renewal effect reported by Bouton and Peck (1989) andBouton and Ricker (1994) and one of the main differences of ourexperiment with those reported by these authors is related with theuse of a context pre-exposure phase before the acquisition train-ing. In their experiments, Bouton and Peck (1989) and Bouton andRicker (1994) always pre-exposed their animals to the contexts thatwere going to be used afterwards in the acquisition, extinction andtest phases. Our findings suggest that such context pre-exposurecould be an important factor to observe the renewal effect, consid-ering that most experiments showing this effect in a wide variety ofprocedures have administered pre-exposure sessions before acqui-sition (e.g. Classical Conditioning: Bouton and Peck, 1989; Boutonand Ricker, 1994; Brooks and Bouton, 1994; Ricker and Bouton,1996; Instrumental Conditioning: Nakajima et al., 2000; Welkerand McAuley, 1978; Conditioned Suppression: Bouton and Bolles,1979; Bouton and King, 1983; Conditioned Taste Aversion: Bernal-Gamboa et al., 2012; Iguchi et al., 2014; Rosas and Bouton, 1998).Experiment 2 was designed to evaluate the effect of the contextpre-exposure phase in an appetitive renewal effect.

3. Experiment 2

Previous experiments by Bouton and colleagues (Bouton andPeck, 1989; Bouton and Ricker, 1994; Brooks and Bouton, 1994)showing ABA renewal in classical appetitive procedures have allused a context pre-exposure phase (i.e. a minimum of 60 min expo-sure to each context to be used), in which subjects were exposedto the conditioning context before the acquisition phase started.Findings in Experiment 1 seem to suggest that pre-exposure phasemay be important to find ABA renewal, perhaps because duringpre-exposure subjects may learn to discriminate between contexts.

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

Therefore, Experiment 2 was designed to assess the effects of con-ducting context pre-exposure with magazine training. Accordingto Bouton and colleagues’ experiments (Bouton and Peck, 1989;Bouton and Ricker, 1994; Brooks and Bouton, 1994), we should be

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Table 3Design of Experiment 2.a

Groups Context pre-exposure Acquisition Extinction Test

ABA Short ABBABAAB A: T+ ITI: 50 s B: T− ITI: 275 s A: T− ITI: 275 sABA Long ABBABAAB A: T+ ITI: 1440 s B: T− ITI: 275 s A: T− ITI: 275 sAAA Short ABBABAAB A: T+ ITI: 50 s A: T− ITI: 275 s A: T− ITI: 275 sAAA Long ABBABAAB A: T+ ITI: 1440 s A: T− ITI: 275 s A: T− ITI: 275 s

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a Note: The A and B characters designate the context where the corresponding phr in absence (−) of the US.

ble to observe ABA renewal, as well as analyze the effect that theTI length used during acquisition has over any subsequent exper-mental phase, regardless of the change to a novel contexts in ABAroups if such a pre-exposure to the contexts is used. In agreement,e suspect that this pre-exposure phase should diminish the neo-hobia that rats experience in novel contexts and will also facilitatehe later discrimination between the contexts used in the differenthases of the experiment.

.1. Method

.1.1. Subjects, apparatus and contextual stimuliThe subjects were 48 experimental naïve Wistar rats (6 male

nd 6 female per group) bred at the same vivarium as those in therevious experiment. They were approximately 90 days old andeighing 195–340 g at the beginning of the experiment. The hous-

ng, food deprivation, apparatus, and all other conditions were theame as those used in Experiment 1, unless otherwise stated.

.1.2. ProcedureThe experimental procedure was almost identical to the Exper-

ment 1 but with the addition of a contextual pre-exposure phase.uring the context pre-exposure phase, which was effective foright sessions, subjects were exposed to both Contexts A and Bsee Table 2) in daily sessions. Each day the subjects were exposedo one of the two contexts in a counterbalanced manner. At theeginning of the session the food-cup was baited with four pre-ision pellets before the rat was located inside the conditioninghamber and there were no further food-deliveries during the restf the session, which lasted 22 min each. After the conclusion ofhis pre-exposure phase, the next phases were identical to thoseescribed in the previous experiment (Table 3).

.2. Results and discussion

.2.1. AcquisitionAccording to the exclusion criteria, one subject of the AAA Short

roup and one of the AAA Long group were eliminated from thetatistical analyses. Panel A of Fig. 2 shows the mean of food-cupntries during the six acquisition sessions. The mean of responses ofoth Short (i.e. AAA Short and ABA Short) and Long (AAA Long andBA Long) groups were collapsed in the same fashion as described

or Experiment 1. It was observed an increase in the mean of theR across the sessions for both Long and Short groups, this find-

ng was confirmed throughout a mixed 2 (ITI Length) × 6 (Session)NOVA (see Table 4), which revealed a reliable main effect ofession and an ITI Length × Session interaction. A planned contrastsnalysis showed that only during the first session were groupsignificantly different, F(1, 264) = 11.59, p < 0.05. In order to ana-yze if this difference was present since the very beginning of therst training session, we conducted an additional analysis of the

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

umber of food-cup entries on the first 30 s of the first acquisi-ion session. This analysis revealed no difference between groups,(1, 44) = 0.003, p > 0.05. An additional analysis during the trialsevealed that this difference was present throughout all session

as conducted, while T stands for the presentation of the tone either in presence (+)

trials for both responses to the CS, F(1, 176) = 37.59, p < 0.05, andduring pre-CS, F(1, 176) = 69.15, p < 0.05. Thus, the length of the ITIsused in each group could produce this difference.

A similar factorial ANOVA analysis for the pre-CS responses (seeTable 4) revealed a main effect of Session and ITI Length factors,suggesting more responding for pre-CS in Group Short, and a differ-ent level of response among sessions. The elevation scores showeda reliable effect for the Session and ITI Length factors, as well asfor the ITI Length × Session interaction. Thus Group Long showeda higher number of food-cup entries than short group during allsessions of the acquisition phase.

During the last acquisition session the mean of food-cup entriesfor the CS were identical for both Short and Long group, as was con-firmed by a planned comparison analysis, F(1, 264) = 0.93, p > 0.05.In contrast, during the pre-CS period it could be observed that ratsthat experienced short ITI lengths during training showed high lev-els of responding than those trained with long ITI lengths. Whenthe elevation scores were calculated, a clear learning curve couldbe observed for the Long group while the Short group remainednear-zero levels of response during the first five sessions of thisphase and then increases to 1.23 responses. Also, it is noteworthythat these results replicate the findings of Experiment 1, becausethe context pre-exposure had no effect in the acquisition of theCR to the CS or to the context. In conclusion, these findings areconsistent with Rescorla and Wagner’s (1972) theory. Once again,when long ITIs are used during training, the context’s associativestrength was extinguished, thus a low level of responding is elicitedby the context in the Long groups. When short ITIs were used how-ever, a high level of responses was observed suggesting a contextualconditioning effect (Sunsay and Bouton, 2008).

3.2.2. ExtinctionPanel B of Fig. 2 shows the mean food-cup entries responses

during the CS and pre-CS periods, as well as the elevation scores foreach of the four groups across the extinction sessions. A reductionof responses was observed as the sessions progressed. This findingwas revealed for the CS-responses by a 2 (ITI Length) × 2 (ExtinctionContext) × 6 (Session) mixed ANOVA (see Table 4), that showed areliable effect of Extinction Context and Session factor, as well as,the interaction between ITI Length × Extinction Context. An addi-tional analysis of this interaction showed that the level of responseto the CS in ABA Long group decreased at a faster rate than the othergroups, for a planned comparison showed differences between AAAand ABA Long groups, F(1, 252) = 14.11, p < 0.05, but not betweenAAA and ABA Short groups, F(1,252) = 0.65, p > 0.05.

The pre-CS responses only revealed a reliable effect for ITILength factor. This finding confirms that Short groups (ABA Shortand AAA Short) responded more during the pre-CS period than Longgroups. However, the main factor of Session was not significant,suggesting that responses during the pre-CS did not change acrossthe extinction sessions. In order to analyze if extinction of the con-

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

ditioned response to context occurred during the first extinctionsession, we conducted an additional analysis using the number ofresponses during each 3 min interval of the first session (i.e. sevenintervals), because the first CS presentation occur at least after

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Fig. 2. Experiment 2: mean responses during the CS, the pre-CS and the ele

00 s. These data revealed an effect of interval, F(6, 294) = 7.20, < 0.05, and an interaction between ITI Length × Interval, F(6,94) = 6.16, p < 0.05. A planned comparison revealed differences

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

etween Short and Long groups only during the first 3 min interval,(1, 294) = 29.70, p < 0.05, suggesting thus that contextual extinc-ion proceed rapidly during the first minutes of the session.

able 4tatistical analysis of Experiment 2.a

Phase Effect

AcquisitionITI Length

Session

ITI Length × Session

ExtinctionITI Length

Extinction Context

Session

ITI Length × Extinction Context

ITI Length × Session

Extinction Context × Session

ITI Length × Extinction Context × Session

TestITI Length

Extinction Context

ITI Length × Extinction Context

a Note: This table shows the F scores of main effects and interactions during acquisition* F scores with p values lower than 0.05.

scores obtained during (A) acquisition, (B) extinction and (C) renewal test.

Elevation scores only showed a reliable effect of ITI Length and ofSession factors. These elevation scores indicate a general decreaseas the phase went on and also show general lower levels of respon-

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

ding for the Short groups compared to the Long groups. However,in contrast with findings of Experiment 1 there were no differencesproduced by the context shift in long groups. Thus, pre-exposure

F scores

CS Pre-CS Elevation score

2.3030 297.9093* 191.7613*

25.7550* 3.2282* 22.8731*

2.2580* 1.01380 4.0506*

0.8388 16.2368* 16.78455*

4.6905* 0.8041 0.8992213.8589* 1.8422 4.50861*

9.7484* 1.0715 3.128940.9825 1.1262 0.735000.1734 1.8092 1.479620.4128 0.4966 0.22569

0.72746 5.10191* 7.531791*

11.99548* 3.37782 4.681845*

0.00030 1.53250 0.983060

, extinction and test of Experiment 2.

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hase eliminated the post-acquisition effect observed in the firstxperiment.

.2.3. Renewal testFinally, panel C of Fig. 2 shows the mean food-cup entries dur-

ng the test session. It was observed that both ABA Short and Longroups increased their responses to the CS during this session, rel-tive to their AAA counterparts. However, ABA Short group alsoncreased the responses to the context. This conclusion was con-rmed by a 2 (ITI Length) × 2 (Extinction Context: ABA vs. AAA)NOVA (see Table 4), that revealed a main effect of the Extinctionontext factor. A planned comparisons revealed significant differ-nces between the groups AAA Short vs. ABA Short, F(1, 42) = 6.06,

< 0.05, and the groups AAA Long vs. ABA Long, F(1, 42) = 5.94, < 0.05.

On the other hand, responding during the pre-CS was highern Short groups than in Long groups. This observation revealed aignificant effect of the ITI Length effect. In order to analyze the dif-erences among groups, we conducted planned comparisons, whichevealed significant differences between AAA Short and ABA Shortroups, F(1, 42) = 4.73, p < 0.05, but not between AAA Long and ABAong Groups, F(1, 42) = 0.18, p > 0.05.

The elevation scores showed a reliable effect of the ITI Lengthnd Extinction Context factors. After conducting planned compar-sons, we found differences between the ABA Long and AAA Longroups, F(1, 42) = 4.98, p < 0.05, but not between ABA Short and AAAhort groups F(1, 42) = 0.69, p > 0.05. These elevation scores suggesthat only the ABA Long group showed a reliable renewal effect.hus, in contrast to the findings of Experiment 1, this experimenthowed a clear contextual renewal effect in the ABA Long group,ut no in the ABA Short group. Additionally, these findings suggesthat context pre-exposure increases the mean of responses to theS during the renewal test, indicating that context pre-exposureould increase the context discriminability (Iguchi et al., 2014).ccording, to Gibson’s (1969) account of perceptual learning, expo-ure to similar stimuli will engage a differentiation process thatill enhance the perceptual effectiveness of the stimulus. It has

een also suggested that alternating pre-exposure is particularlyffective in maintaining or strengthening the effectiveness of twoues, because these cues are presented according to a schedule thatromotes comparison between them. In agreement, Thomas et al.2003) have showed that renewal effect it is not observed when And B context differ only in terms of odor.

Results of Experiment 2 also show that ABA Short group had high level of responses to the CS, as well as, during the pre-CScross the acquisition phase. These findings are in agreement withhe proposal of Rescorla and Wagner (1972) that suggests the estab-ishment of stronger Context–US associations in Short groups thann Long groups.

Additionally, results of the test session (Fig. 2, panel C) show twonteresting findings. First, those groups extinguished in context Bave a high level of responses to the CS than those extinguished inontext A. Second, only the ABA Short group showed a high level ofesponses to the context. Since all groups received the extinctionf the CS, the first and the second findings of ABA Short suggesthat context could establish direct context–US associations. Addi-ionally, results of ABA Long group showed an increase in the levelf responses only to the CS, thus this group shows that the con-ext has modulatory role. In conclusion, these results suggest thatontext could establish a hierarchical relationship with the CS–USssociations, as well as, direct associations between context and US;hich is in agreement with some proposals that give to the con-

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

exts two different functions across a conditioning task (Urcelaynd Miller, 2010, 2014). The first function is that the context devel-ps a direct association with the US. Thus when the CS is presenteduring acquisition, the CS and the context may get conditioned in a

PRESS Processes xxx (2014) xxx–xxx

similar manner (Miller and Matzel, 1988; Miller and Schachtman,1985; Rescorla and Wagner, 1972; Wagner, 1981). For example,it has been shown that US pre-exposure delays the acquisition ofthe CS–US association (e.g. Tomie, 1976). According to Rescorlaand Wagner (1972), during the US pre-exposure phase, subjectslearn a Context–US association, which blocks the acquisition of anew CS–US association. In other words, the Context–US associa-tion formed during the US pre-exposure is capable of blocking theCS conditioning (e.g. Kamin, 1969).

Even though these results show ABA renewal for the ABA Longgroup, it is not possible to reliably evaluate the mechanism thatproduces such renewal. Until now there are several explanations tothis phenomenon. In first place, at least in ABA renewal, it could besuggested that the associative strength of the context summatedwith the residual associative strength of the CS to produce therenewal effect (Balaz et al., 1981a, 1981b; Bouton, 1984; Milleret al., 1988). Alternatively, Bouton (1993) suggests that the con-text develops a modulatory role during the extinction phase andthis modulatory effect is assumed to be responsible of the renewaleffect because in all renewal designs a change in the extinctionand test context must occur. According to this perspective, theresponse recovery observed in the renewal test occurs because theextinction context is not present to exert its modulation over theanimal’s behavior. According to this line of thought any renewaleffect should generate the same level of response recovery, regard-less of the particular renewal design used (i.e. ABA, AAB and ABC;see Thomas et al., 2003). Finally, Urcelay and Miller (2010, 2014)have recently proposed that the contexts can develop associativestrength, as well as, modulatory or occasion setting propertiesdepending on the length of the ITI used during the training in suchcontext. In their experiments, they found that short ITIs facilitatethe formation of Context–US associations whereas the long ITIsfacilitate the modulatory properties of the context. Some experi-ments contrasting ABA, ABC and AAB renewal designs in differentprocedures (e.g. fear conditioning, Thomas et al., 2003; instrumen-tal conditioning, Bouton et al., 2012) have shown that ABA renewaleffect is significantly stronger than AAB and ABC renewal. In agree-ment, it can be supposed that this difference could be producedby summation of the associative strength of the context with theresidual associative strength of the CS (Rescorla and Durlach, 1987;Rescorla and Wagner, 1972). Thus, if the associative strength ofthe acquisition context is extinguished before the renewal test, weshould observe an attenuation of the renewal effect, but if contextis having a role of occasion setter, as has been suggested by Urcelayand Miller (2010, 2014) the extinction of the acquisition contextshould not have any effect on the contextual renewal.

Results of groups ABA and AAA short revealed, during the testsession to the context, higher levels of responding during the pre-CS and the CS in ABA than in AAA groups. These findings could beexplained at least in two different ways. First, the informative the-ory proposed by Egger and Miller (1962) could suggest that the CSand the context are equally reliable predictors of the US when sub-jects were trained with short ITIs, thus context will acquire moreassociative strength, since the CS is a redundant cue. Additionally,it is possible to conceive the acquisition phase as an overshadowingphase where the context and the CS competed for the associativestrength with the US (Kamin, 1969). An alternative explanationof overshadowing suggests that this phenomenon is produced bya retrieval failure, rather than impairment in the acquisition ofassociative strength (Matzel et al., 1985). In agreement, Kaufmanand Bolles (1981) reported a recovery from overshadowing whenthe association between the overshadowing stimulus and the US

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

was extinguished. These results suggest that both stimuli in anovershadowing procedure acquire associative strength. In Exper-iment 2 the extinction of the CS did not produce any effect incontextual conditioning during the test, however, the experiments

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escribed above always extinguished the overshadowing stimulusi.e. CS). Therefore, if the context’s associative strength is extin-uished before the test phase, we should observe a decrease in there-CS responses, as well as, an increase in the level of response tohe CS. However, recovery of the overshadowed stimulus has beenound using different aversive procedures (Kaufman and Bolles,981; Balaz et al., 1982; Kasprow et al., 1982; Matzel et al., 1985),hile Holland (1999) did not found this effect with appetitive pro-

edures.

. Experiment 3

Urcelay and Miller (2010) suggested that using different ITIengths on certain context dependent procedures seems to deter-

ine whether the context acquires characteristics similar to thosef a discrete stimulus (CS) or to those of a modulator (i.e., anccasion setter). Following this reasoning and starting from theifferential contextual conditioning effect observed in the previ-us experiment, Experiment 3 was aimed to assess in a more directanner the view that using the parameters and procedure of Exper-

ment 2, will promote that the acquisition context will functions a CS when short ITI lengths are used, but not when longer ITIengths are employed. It is important to note that the pre-exposurehase in Experiment 2 seemed to allow this differential effect toecome measurable, so we kept this phase in this experiment. Inrder to assess the CS properties of the context, we added con-ext extinction sessions during the CS extinction phase in the sameBA renewal paradigm of Experiment 2. If the acquisition con-

ext actually has CS properties when trained with short ITI lengths,mposing these context extinction sessions for Context A shouldause this context’s associative strength to diminish and therefore,he differential effect of Experiment 2 should also be attenuatedor all subjects that experience such context extinction session ofhe acquisition context (i.e. Context A). In addition, if these con-ext extinction sessions are not conducted in the context wherehe acquisition phase took place (i.e. Context B); we expect to repli-ate the results obtained in Experiment 2, because the associativetrength accrued by the acquisition context (Context A) shouldemain unaffected.

.1. Method

.1.1. SubjectsThe subjects were 48 experimental naïve Wistar rats (6 male

nd 6 female per group) bred at the same vivarium as those inrevious experiments. They weighed 191–351 g at the beginningf the experiment. The housing, food deprivation, CS and US werehe same as those used in Experiment 1. Due to illness, one rat ofroup BB Long had to be excluded from the experiment.

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

.1.2. ApparatusExperimental sessions were conducted in eight conditioning

hambers with the same form, size and configuration of those usedn previous experiments.

able 5esign of Experiment 3.a

Groups Context pre-exposure Acquisition Extinction

CS

BA-S ABBABAAB A: T+ ITI: 50 s B: T− ITBA-L ABBABAAB A: T+ ITI: 1440 s B: T− ITBB-S ABBABAAB A: T+ ITI: 50 s B: T− ITBB-L ABBABAAB A: T+ ITI: 1440 s B: T− IT

a Note: The A and B characters designate the context where the corresponding phase wr in absence (−) of the US.

PRESS Processes xxx (2014) xxx–xxx 9

4.1.3. Contextual stimuliThe eight conditioning chambers constituted a matrix of 4 rows

by 2 columns. In order to conduct the experimental sessions, theconditioning chambers were adapted to provide two different anddistinctive contexts. These contexts differed on their olfactory, tac-tile and location features between them, and these features weredifferent from those used in Experiments 1 and 2 because otherexperiments were conducted concurrently in the lab, and suchexperiments required different contextual features from those par-ticularly used in the previous experiments. Both contexts werecounterbalanced for all subjects.

The four chambers of the two upper rows (Context Vinegar-Foamy) had the floor of the boxes covered with a sheet of whitevinyl acetate ethylene (Barrilito® White Foamy) and a containerwith 15 ml of acetic acid (Cane Alcohol’s White Vinegar ClementeJacques®, SABORMEX S.A. de C.V., D.F., México) was also placedunder the food-cup. In the other hand, the four chambers in thetwo lower rows (Context Fruits-Cardboard) had the floor coveredwith a sheet of pale yellow cardboard (SuperFile Folders®, IrasaIndustrial S.A. De C.V., D.F., México) and a container with 15 ml ofliquid cleaner FABULOSO Fruit Explosion® (Colgate-Palmolive, S.A.de C.V., D.F., México) was also placed under the food-cup. The olfac-tory and tactile stimuli used in each context were replaced everytwo days.

4.1.4. ProcedureThe experimental sessions were conducted using the same pro-

tocol of Experiment 2 and consisted of four phases: pre-exposure,acquisition, extinction (to the CS and to the context) and test. Thepre-exposure and acquisition phases were the same as those phasesof Experiment 2 (see Table 5).

Following pre-exposure and acquisition, the extinction phasewas conducted for 6 days and each day consisted in 2 daily ses-sions, one identical to the extinction sessions of Experiment 2 (i.e.CS extinction) and another where subjects were exposed to theacquisition context (Context A) or to the extinction context (Con-text B). The reason for using this control groups that are exposedto the extinction context during this second daily session wasto equate the additional exposure the other groups were receiv-ing in the acquisition context. Thus if any difference is observedwe can reliably assume such difference is due to the extinctionof the acquisition context’s associative strength and not due tothe difference in total exposure to the experimental chambersduring this phase. These sessions lasted approximately 22 mineach and there were no CS or US presentations. These extinc-tion sessions for each group were spaced by an inter-sessioninterval or ISI (i.e. from the end of the CS extinction sessionto the start of the Context extinction session) of approximately40 min.

Finally, all groups were tested the same day with two inde-

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

pendent test sessions, the first one in the acquisition contextand the second one in the extinction context. The order of suchsessions was not counterbalanced. The ISI was of approximately40 min.

Test A Test B

Context

I: 275 s A: − A: T− ITI: 275 s B: T− ITI: 275 sI: 275 s A: − A: T− ITI: 275 s B: T− ITI: 275 sI: 275 s B: − A: T− ITI: 275 s B: T− ITI: 275 sI: 275 s B: − A: T− ITI: 275 s B: T− ITI: 275 s

as conducted, while T stands for the presentation of the tone either in presence (+)

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Fig. 3. Experiment 3: mean responses during the CS, the pre-CS and the ele

.2. Results and discussion

.2.1. AcquisitionOn the basis of the above-mentioned exclusion criteria, one sub-

ect of group BA-S and one of group BB-L were excluded from allnalyses. The learning curve of the acquisition phase of all groupss presented in panel A of Fig. 3. The responses of the groups wereollapsed in the same fashion as in Experiments 1 and 2, dependingn the mean ITI length that they experienced. For the CS responses,e used a mixed 2 (ITI Length) × 6 (Session) ANOVA (see Table 6),

hat revealed a reliable effect of the Session factor. A similar anal-sis was conducted for the pre-CS responses and revealed a mainffect of the Session and ITI Length factors, as well as the interactionetween these factors. When the elevation scores were analyzed,e observed the same main effects of Session and ITI Length factors,

s well as their interaction.Once again, we replicated the acquisition curves observed in

xperiments 1 and 2, for both the CS and for the pre-CS responses,s well as for the elevation scores of all groups. These scores showhe same increase on the level of responding while the tone wasresent regardless the ITI length used during the acquisition ses-ions and, during the pre-CS period the rats that experienced shortTI lengths showed high levels of responding but those that expe-ienced long ITI lengths did not. Elevation scores also showed ancquisition curve for the Long group while the scores of the Shortroup remained at levels near to zero.

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

.2.2. CS and context extinctionPanel B of Fig. 3 shows the response decrease of the four groups

uring the CS extinction phase. We used a mixed 2 (ITI Length) × 2

scores obtained during (A) acquisition, (B) extinction and (C) renewal test.

(Extinguished Context [A or B]) × 6 (Session) ANOVA to analyze theCS responses (Table 6). The ANOVA only revealed a reliable effectof the Session factor. In the case of the pre-CS responses it wasfound a reliable effect of the ITI Length and of the Session fac-tors, as well as an ITI Length × Extinguished Context and an ITILength × Session interactions. A more detailed analysis of the ITILength × Extinguished Context interaction showed that the BB-Lgroup differed significantly from the other three groups, suggestingthat the Long group receiving two extinction sessions in Con-text B had the lowest level of responses. While short groups, aswell as, BA-L showed similar level of responses during the pre-CS. The ANOVA for the elevation scores yielded reliable effectsfor the ITI Length and Session factors, as well as for their inter-action. A planned comparison analysis showed that Short groupssignificantly differ from Long groups, BA-S vs. BA-L, F(1,246) = 8.94,p < 0.05, BB-S vs. BB-L, F(1,246) = 11.70, p < 0.05. Even short and longgroups differed during the first five extinction sessions, during thelast extinction session no differences were observed among groups,F(1, 246) = 20.30, p < 0.05, and the session, F(1, 246) = 0.79, p > 0.05.

Fig. 4 shows the decrease in responding by the four groups dur-ing the first and the last sessions of those sessions where contextwas extinguished. Since there was neither CS nor US presentationin these sessions, the results are displayed in the mean of food-cupentries every 3 min (i.e. 3 min Intervals). A mixed 2 (ITI Length) × 2(Extinguished Context) × 7 (Interval) ANOVA to the first sessiondata revealed a main effect of ITI Length, F(1, 287) = 48.56, p < 0.05,

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

of Extinguished Context, F(1, 287) = 24.84, p < 0.05, and of Interval,F(6, 287) = 11.20, p < 0.05; as well as for the ITI Length × Intervalinteraction, F(6, 287) = 3.07, p < 0.05. A planned comparisons duringthe first interval of this first session, revealed significant differences

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Table 6Statistical analysis of Experiment 3.a

Phase Effect F scores

CS Pre-CS Elevation score

AcquisitionITI Length 0.1301 168.8544* 145.3457*

Session 18.6881* 6.3789* 12.2064*

ITI Length × Session 1.0883 4.6714* 6.3259*

ExtinctionITI Length 0.2867 31.2479* 20.57572*

Extinguished Context 0.9999 0.8229 0.01059Session 14.0187* 2.4989* 4.69121*

ITI Length × Extinguished Context 3.8273 5.7687* 0.13154ITI Length × Session 0.3463 2.5041* 3.03353*

Extinguished Context × Session 0.4786 0.2886 0.75326ITI Length × Extinguished Context × Session 0.8906 0.2793 0.58475

TestExtinguished Context 1.9327 0.72784 0.45875Test Context 51.4730* 3.30393 25.94383*

ITI Length 7.0439* 0.32945 7.04772*

Extinguished Context × Test Context 4.3832* 1.35608 1.19765Extinguished Context × ITI Length 0.1333 0.86839 0.06744Test Context × ITI Length 4.9909* 0.06896 4.40288*

Extinguished Context × Test Context × ITI Length 0.0862 3.14964 1.83

isition

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a Note: This table shows the F scores of main effects and interactions during acqu* F scores with p values lower than 0.05.

etween the BA Short vs. BB Short groups, F(1, 287) = 8.29, p < 0.05,he BA Long vs. BB Long groups, F(1, 287) = 8.29, p < 0.05, the BAhort vs. BA Long groups, F(1, 287) = 20.80, p < 0.05, and the BB Shorts. BB Long groups, F(1, 287) = 13.81, p < 0.05. This pattern suggestsifferences among all the groups, meaning that both the contextnd the ITI length used during the acquisition sessions affect theevel of response. Thus, training with long ITIs produce the low-st level of response to the context, while using short ITIs result inigh level of response. Additionally, when the acquisition context

s presented (i.e. context A) a higher number of food-cup entriesere registered in BA groups than in BB groups. In conclusion, thesendings confirm a higher level of contextual conditioning in Shortroups than in Long groups, in agreement with those experimentshowing different associative strength when short and long ITIs aresed (e.g. Sunsay and Bouton, 2008).

The results of the last session of extinction were analyzed with mixed 2 (ITI Length) × 2 (Extinguished Context) × 7 (Interval)NOVA which showed a main effect of the Extinguished Context,(1, 287) = 22.00, p < 0.05, and of Interval, F(6, 287) = 2.80, p < 0.05,

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

s well as for the ITI Length × Extinguished Context interaction,(1, 287) = 6.77, p < 0.05. A planned comparison was conducted forhe last interval of the session and it showed no reliable differencesetween groups, F(1, 287) = 1.44, p = 0.2313. In brief, these results

Fig. 4. Experiment 3: mean responses of each 3-min bins during the first

, extinction and test of Experiment 3.

suggest that the level of response to the food-cup decreasedsignificantly across the extinction sessions, so that the level ofresponses registered in the last 3-min interval of the last sessiondid not differ among groups.

4.2.3. Renewal testFinally, the responses of the test phase are depicted in the panel

C of Fig. 3. A factorial 2 (ITI Length) × 2 (Extinguished Context)ANOVA (Table 6) was conducted for the responses to the CS in thetest session conducted in Context A. This analysis showed a maineffect of the ITI Length factor. When the responses during the pre-CS were analyzed, neither the main effects, nor the interactionswere significant. Finally, this analysis using the elevation scoresshowed significant differences only for the main factor ITI length. Aswell as, with the responses to the CS, this analysis showed neitherdifference between BA-S and BB-S groups, F(1, 41) > 0.01, p > 0.05,and between BA-L and BB-L groups, F(1, 41) = 1.69, p > 0.05. Thus,our results did not show any effect of the extinction of Context–USassociations in level of responses registered during the test in the

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

acquisition context.In order to establish if we were observing a contextual renewal

effect, we contrasted the elevation scores observed in Context Aagainst those registered in Context B. A mixed 2 (Test Context) × 2

(left panel) and the last (right panel) context-extinction sessions.

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ITI Length) × 2 (Extinguished Context) ANOVA showed significantifferences for the main factors ITI Length, F(1, 82) = 7.05, p < 0.05,nd Test Context, F(1, 82) = 25.84, p < 0.05, as well for the interactionTI Length × Test Context, F(1, 82) = 4.40, p < 0.05. A planned com-arison analysis did not showed any difference between responseso context A and B in BA-S group, F(1, 82) = 2.60, p > 0.05, in BB-

group, F(1, 82) = 2.01, p > 0.05, however, the BA-L group, F(1,2) = 6.04, p < 0.05, and BB-L, F(1,82) = 20.76, showed that they dif-ered significantly in the level of response between context. Inonclusions, these data shows contextual renewal only when sub-ects were trained with ITIs of long length.

. General discussion

As stated in the introduction, less research regarding renewalhenomena has been made with appetitive conditioning pro-edures in comparison with the widely addressed aversiveonditioning literature. Such procedure was used in this exper-mental series. In the acquisition phase of all Experiments, we

ere able to obtain similar acquisition curves for the CS responsesegardless of what ITI length was used in this training. Conversely,nly the Short groups revealed high levels of conditioned respon-ing to the pre-CS period during this phase. In other words, the toneas equally conditioned in all groups by the end of the acquisitionhase but only the rats trained with a mean ITI of 50 s showedigh levels of food-cup entries during the pre-CS period as well,hich may be indicative of contextual conditioning. Nevertheless

his assumption was not entirely conclusive, because the animalsn the ABA groups of Experiment 1 showed high levels of pre-CSesponses at the beginning of the extinction phase and the renewalest yielded no response recovery whatsoever in either responsecore (i.e. CS or pre-CS). These results are consistent with the find-ngs of Sunsay and Bouton (2008) and Mustaca et al. (1991) in thathey report higher pre-CS responses when short ITIs are used.

In Experiment 2, we effectively eliminated the exploratoryehavior observed during the first extinction session, by pre-xposing the animals to both contexts before the start of thecquisition phase. Despite this pre-exposure phase, we replicatedur acquisition curves both for CS and pre-CS responses. In thisxperiment the subjects in the ABA groups had significantly lowerevels of pre-CS responses at the start of the extinction phase thanhose in AAA groups. These results show that the pre-CS responsesf the groups AAA are not elicited by exploratory behavior but iteems to be the conditioned response generated by the trainingontext and constitute an example of the post-acquisition effect.he post-acquisition effect consists in an abrupt decrease of the CRhen organisms undergo extinction in a different context from thatsed in acquisition, compared with subjects that receive extinc-ion treatment in the same context of training (Nakajima et al.,000). In the other hand, when elevation scores were measured,o difference was found between the Long groups, in contrast tohe difference observed in Experiment 1. These results suggest thathe post-acquisition effect was eliminated due to the pre-exposurehase used in Experiment 2. Finally in the renewal test we were ableo find a response recovery in the CS responses of both ABA groups,ut more importantly, we also obtained a reliable recovery of there-CS score only in the group ABA Short which seems to be theesult of the context associative strength that was protected fromxtinction when the subjects of this group experienced extinctionn a different context (i.e. Context B). These findings provide evi-ence that contextual conditioning occurs during acquisition if the

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

emporal parameters are adequate and more importantly this con-extual conditioning does not seem to summate at the moment ofhe renewal test (see also Todd et al., 2012; Bouton et al., 2012 forimilar results showing no contextual summation).

PRESS Processes xxx (2014) xxx–xxx

Experiment 3 allowed us to assess directly the acquisition-context conditioning by deliberately exposing this context duringextinction without any stimuli presentation (i.e. either CS or US)in order to extinguish any associative strength that it may hadacquired during training. Indeed the rats that were exposed to Con-text A during extinction failed to show the same renewal effects ofExperiment 2. Also the analysis of the response cessation duringthe context-extinction phase allowed us to detect and replicate aneffect indirectly reported by Sunsay and Bouton (2008), which isthat the rats conditioned with shorter ITIs tended to execute moreresponses per unit of time than the rats that were trained withlonger ITIs. Apparently, the temporal distribution of the trials dur-ing training affects the general response rate that the subjects willacquire. It is noteworthy that the six sessions of contextual extinc-tion that the organisms underwent concurrently with the regularCS extinction sessions was insufficient to completely eliminate theresponses elicited by the context, as the analysis of the last con-textual extinction session revealed. It is logical to suppose that theresults of the test phase in this experiment, particularly those ofthe BA-S and BB-S groups may be affected, at least in part, by thisunextinguished context responses.

Regarding the elevation scores of the renewal test, these resultsare readily explained by the information retrieval model (Bouton,1993), since only the groups that showed learning during acquisi-tion (i.e. L groups) had reliable recovery of responses as a result ofthe context shift between extinction and test despite the contextthat was further extinguished (i.e. contextual extinction). Also, thelack of differences between the CS scores and elevation scores of theBA-S and BB-S groups during the renewal test could have happendue to retrospective revaluation of the CS predictive value after theCS and Contextual extinction sessions (e.g. Miller et al., 1992; butsee Holland, 1999), thus eliminating any difference in the originalconditioned responses to the CS in this groups.

The present results are interesting in several accounts. First ofall, as it has been pointed out before, there is relatively not muchdata about renewal in appetitive procedures since most of theresearch in this area has been conducted mainly with aversive pro-cedures (e.g. conditioned suppression, conditioned taste aversion,fear conditioning). An interesting result is the fact that the con-textual conditioning observed in the groups Short did not seem tointerfere with the conditioning of the tone in none of our exper-iments. In a previous set of experiments Urushihara and Miller(2009) explored the cue competition effect considering the trainingcontext as one of the competing cues. The cue competition effectis generally described as the competition between several stimulito gain the behavioral control. Rescorla and Wagner (1972) modelexplains this competition as the result of the division of the out-come’s associative strength among the present stimuli (see alsoVan Hamme and Wasserman, 1994; Wagner, 1981). Following thislogic, all of these models predict an inverse relationship betweenthe behavioral control accrued by a stimulus in relationship to theother stimulus. In the other hand, the comparator hypothesis pre-dicts the cue competition effect as the result of interaction at thetime of behavioral expression (Urushihara and Miller, 2009). Thus,the comparator hypothesis generates the prediction that when theassociation between the stimuli changes, the behavioral control ofone of the stimuli is expected to change in the same direction asthat of the other cue. In their experiments, Urushihara and Miller(2009) explored the relationship between two competing stimuli(i.e. a CS and the Context) and the total reinforcer value impartedby a constant US. They observed a decrease in responding to bothstimuli, thereby supporting the view of the comparator hypothesis

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

over the tradeoff traditional view. Similarly, in all our experiments,all groups showed similar extinction curves for the CS responsesindependently of the context used during such phase. If the CS andthe Context would compete with each other during acquisition in

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rder to gain associative strength for the organisms of the Shortroups, a tradeoff between them must have taken place. Still, simi-ar extinction curves between ABA and AAA groups were observed.his lack of cue competition between the acquisition context andhe tone does not follow the predictions of the Rescorla and Wag-er’s model which predict a decrease in the associative strengthf the tone for those subjects trained with short ITIs, since thecquisition context should have gained more associative strength,ompared with those trained with longer ITIs. Still, the pre-CSesponses observed in all Short groups may not be result of con-extual conditioning since these responses were eliminated evenhen a different context was extinguished, as seen in Experiment

. Even though the present results do not show evidence of con-extual summation whatsoever, contextual conditioning may beesponsible in other procedures of investigating renewal. Severalesearchers (e.g. Nakajima et al., 2000; Thomas et al., 2003; Üngornd Lachnit, 2008; Carranza-Jasso et al., unpublished results) haveointed out that some procedures elicit different levels of responseecovery when tested with all the renewal designs (i.e. ABA, AABnd ABC).

There is an additional perspective that can explain the presentesults. It is possible that the short ITIs promoted the tone and theontext to be associated as a single compound stimulus (e.g. Pearce,987). In Experiment 1, the context accompanied by the CS, the con-ext alone and the CS alone may have been taken as the same CS dueo generalization, causing that the organisms to behave similarlyhroughout the experiment regardless of the context used duringxtinction. In Experiment 2, the pre-exposure phase could haveelped the organisms to better discriminate between the elemen-al stimuli and the compound stimulus later introduced during thecquisition phase. Finally in Experiment 3, the additional extinc-ion sessions had no effect over the compound stimuli, generatingimilar outcomes to the BA-S and BB-S groups. Unfortunately ourrocedure does not let us assess if such configural stimulus was

ndeed operating with this design. One possible way to determinef such representation is formed would be to replicate these proce-ures with an additional test in a neutral context. If any responsebserved during the test in the acquisition context is seen by meansf a compound (e.g. CS + Context) stimulus, then such responseshould not be seen when those organisms are tested in a neutralontext (e.g. Context C).

Finally, as mentioned before, the most successful model usedo explain these response recovery phenomena is the informa-ion retrieval model (Bouton, 1993). A main assumption of this

odel is that the organisms will only learn about the context untilhe extinction phase because of the ambiguity of the CS’ informa-ive value. Following this idea, there should not be any contextualonditioning during acquisition because in this phase, there is nombiguity in the informative value of the CS. Despite this pre-iction, we were able to demonstrate in all of our experimentshat contextual conditioning could be acquired if the proper ITIength was used (e.g. 50 s) even though there was no ambiguity

hatsoever during this phase. This results are in line with Urcelaynd Miller (2010, 2014, see also Urcelay et al., 2012) findings in

task where they trained rats with short or long ITIs in US pre-xposure or proactive interference procedures and showed that

variable of outmost importance determining the contexts func-ion in such learning tasks are the ITI lengths. However additionalesearch should be conducted in order to adequately determine ifhe high levels of pre-CS responses are indeed result of contextualonditioning.

An important limitation of the present experiments is that we

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

ocused in the CS role of the context in this procedure, thus wead no design manipulation to assess if long ITIs facilitate occa-ion setting properties of the context in the same way that shortTIs facilitate CS properties. A future research effort should be to

PRESS Processes xxx (2014) xxx–xxx 13

determine if such occasion setting facilitation occurs with long ITIsin this appetitive preparation. Another possible limitation is thatmassed training appears to generate little conditioning to the CS asmeasured by the Elevation Score, which makes it difficult to reliablyassess extinction and renewal.

In summary, the results of the experiments reported in thispaper give several important contributions. First we found that acontext pre-exposure phase is imperative in order to obtain the ABArenewal effect in an appetitive pavlovian conditioning procedure.When we added such a pre-exposure phase prior to the acquisitionphase, we were able to successfully observe a renewal effect, whichwas completely absent when the same procedure was conductedwithout the pre-exposure phase. The importance of a pre-exposurephase in order to observe the renewal effect is somewhat unpre-dicted by the information retrieval model (Bouton, 1993), whichstates as only requirement that there must be a context changebetween the extinction and test phase for the renewal effect to beobserved. Apparently, the novelty of the contexts used during therenewal procedure is also an important variable that determinesthe expression or the lack of an observable renewal effect. Sec-ond, we were able to find a general contextual conditioning effectwhen the organisms were trained with relatively short ITIs (i.e.50 s mean length). Also this contextual conditioning had as resultnear-zero elevation scores throughout the experiment, which maybe interpreted as a lack of conditioning in the Short groups of allthe experiments. Also we found that relatively long ITIs (i.e. 1440 smean length) are needed to obtain a reliable renewal effect using anappetitive pavlovian conditioning procedure. Finally, the results ofExperiment 3 show that directly extinguishing the acquisition con-text successfully reduced the pre-CS responses at the ABA renewaltest of the group trained with short ITIs, but this reduction hadno reliable effect over the elevation scores of this group in thesame test. This pattern of results suggest that even though con-textual conditioning occurs when organisms are trained with shortITIs, such contextual conditioning does not interfere with the finalbehavioral outcome at the renewal test.

It is worth noting that these results may help to understandwhy some drug abuse or phobic patients relapse even when theirtherapists adopt strategies to prevent such relapse. One possibil-ity is that even after extensive extinction of the CS, the simpleexposure to the environment where they learned their addictionor phobia may be enough to relapse because of context condition-ing if they first learned such maladaptive behavior with relativelymassed trials. Yet, this is just a venturesome hypothesis and stillmuch more research in this relatively unknown subject must beconducted before any forceful affirmation can be made.

Acknowledgments

The experiments depicted in this article are part of RodrigoCarranza-Jasso’s doctoral dissertation and they are published infulfillment of the requirements for the PhD degree. This researchwas funded by the Graduate Studies Scholarship Program (Schol-

arship #249617) of the Consejo Nacional de Ciencia y Tecnología(CONACYT) granted to Rodrigo Carranza-Jasso, and by the Programade Apoyo a Proyectos de Investigación e Innovación Tecnológica(PAPIIT) projects IN307413 granted to Dr. Livia Sánchez-Carrascoand IN304411 granted to Dr. Javier Nieto. We would like tothank Alexis Martínez-Ramírez, Alma Delia Pérez-López and ArletteCarrillo-Sulub for helping with the conduction of the experimentalsessions.

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

References

Balaz, M.A., Capra, S., Hartl, P., Miller, R.R., 1981a. Contextual potentiation ofacquired behavior after devaluing direct Context–US associations. Learn. Motiv.12, 383–397.

1145

1146

1147

1148

ING ModelB

1 ioural

B

B

B

B

BQ4

B

B

B

B

B

B

B

B

B

B

B

C

C

C

D

E

G

G

G

H

H

I

K

K

K

ior. In: Spear, N.E., Miller, R.R. (Eds.), Information Processing in Animals: MemoryMechanisms. Erlbaum, Hillsdale, NJ, pp. 5–47.

1149

1150

1151

1152

1153

1154

1155

1156

1157

1158

1159

1160

1161

1162

1163

1164

1165

1166

1167

1168

1169

1170

1171

1172

1173

1174

1175

1176

1177

1178

1179

1180

1181

1182

1183

1184

1185

1186

1187

1188

1189

1190

1191

1192

1193

1194

1195

1196

1197

1198

1199

1200

1201

1202

1203

1204

1205

1206

1207

1208

1209

1210

1211

1212

1213

1214

1215

1216

1217

1218

1219

1220

1221

1222

1223

1224

1225

1226

1227

1228

1229

1230

1231

1232

1233

1234

1235

1236

1237

1238

1239

1240

1241

1242

1243

1244

1245

1246

1247

1248

1249

1250

1251

1252

1253

1254

1255

1256

1257

1258

1259

1260

1261

1262

1263

1264

1265

1266

1267

1268

1269

1270

1271

1272

1273

1274

1275

1276

1277

1278

1279

1280

1281

1282

1283

1284

1285

1286

1287

1288

1289

1290

1291

1292

1293

1294

1295

1296

1297

1298

ARTICLEEPROC 2861 1–14

4 R. Carranza-Jasso et al. / Behav

alaz, M.A., Capra, S., Kasprow, W.J., Miller, R.R., 1981b. Latent inhibition of theconditioning context: further evidence of contextual potentiation of retrievalin the absence of appreciable Context–US associations. Anim. Learn. Behav. 12,383–397.

alaz, M.A., Gutsin, P., Cacheiro, H., Miller, R.R., 1982. Blocking as a retrieval failure:reactivation of associations to a blocked stimulus. Quart. J. Exp. Psychol. 34 (2),99–113.

alderas, I., Rodriguez-Ortiz, C.J., Salgado-Tonda, P., Chavez-Hurtado, J., McGaugh,J.L., Bermudez-Rattoni, F., 2008. The consolidation of object and context recog-nition memory involve different regions of the temporal lobe. Learn. Mem. 15(9), 618–624.

arela, P.B., 1999. Theoretical mechanisms underlying the trial-spacing effect inpavlovian fear conditioning. J. Exp. Psychol. Anim. Behav. Process. 25, 177–193.

arnett, V., Lewis, T., 1994. Outliers in Statistical Data, 3rd ed. John Wiley and Son,pp. 582.

ernal-Gamboa, R., Juárez, Y., González-Martín, G., Carranza, R., Sánchez-Carrasco, L.,Nieto, J., 2012. ABA, AAB and ABC renewal in taste aversion learning. Psicológica33 (1), 1–13.

onardi, C., Honey, R.C., Hall, G., 1990. Context specificity of conditioning in flavor-aversion learning: extinction and blocking tests. Anim. Learn. Behav. 18 (3),229–237.

outon, M.E., 1984. Differential control by context in the inflation and reinstatementparadigms. J. Exp. Psychol. Anim. Behav. Process. 10, 56–74.

outon, M.E., 1993. Context, time and memory retrieval in the interferenceparadigms of pavlovian learning. Psychol. Bull. 114 (1), 80–99.

outon, M.E., Bolles, R.C., 1979. Contextual control of the extinction of conditionedfear. Learn. Motiv. 10 (4), 445–466.

outon, M.E., King, D.A., 1983. Contextual control of the extinction of conditionedfear: tests for the associative value of the context. J. Exp. Psychol. Anim. Behav.Process. 9, 248–265.

outon, M.E., Peck, C.A., 1989. Context effects on conditioning extinction, and rein-statement in an appetitive conditioning preparation. Anim. Learn. Behav. 17,188–198.

outon, M.E., Rosengard, C., Achenbach, G.G., Peck, C.A., Brooks, D.C., 1993. Effectsof contextual conditioning and unconditional stimulus presentation on perfor-mance in appetitive conditioning. Quart. J. Exp. Psychol. Sect. B: Comp. Physiol.Psychol. 46 (1), 63–95.

outon, M.E., Ricker, S.T., 1994. Renewal of extinguished responding in a secondcontext. Anim. Learn. Behav. 22, 317–324.

outon, M.E., Winterbauer, N.E., Todd, T.P., 2012. Relapse processes after the extinc-tion of instrumental learning: renewal, resurgence, and reacquisition. Behav.Process. 90, 130–141.

rooks, D.C., Bouton, M.E., 1994. A retrieval cue for extinction attenuates responserecovery (renewal) caused by a return to the conditioning context. J. Exp.Psychol. Anim. Behav. Process. 20 (4), 366–379.

ampese, V., Delamater, A.R., 2013. ABA and ABC renewal of conditioned magazineapproach are not impaired by dorsal hippocampus inactivation or lesions. Behav.Brain Res. 248, 62–73.

arranza-Jasso, R., Martínez, M., Sánchez-Carrasco, L., 2014. ABA, AAB and ABCrenewal in appetitive pavlovian conditioning (Unpublished results).

ole, K.C., VanTilburg, D., Burch-Vernon, A., Riccio, D.C., 1996. The importance ofcontext in the US preexposure effect in CTA: novel versus latently inhibitedcontextual stimuli. Learn. Motiv. 27, 362–374.

enniston, J.C., Chang, R.C., Miller, R.R., 2003. Massive extinction treatment attenu-ates the renewal effect. Learn. Motiv. 34, 68–86.

gger, M.D., Miller, N.E., 1962. Secondary reinforcement in rats as function of infor-mation value and reliability of the stimulus. J. Exp. Psychol. 64 (2), 97–104.

allistel, C.R., Gibbon, J., 2000. Time, rate, and conditioning. Psychol. Rev. 107,289–344.

ibbon, J., Balsam, P., 1981. Spreading associations in time. In: Terrace, H.S., Gibbon,J. (Eds.), Autoshaping and Conditioning Theory. Academic Press, New York.

ibson, E.J., 1969. Principles of Perceptual Learning and Development, 1st ed.Appleton-Century-Crofts, New York.

olland, P.C., 1999. Overshadowing and blocking as acquisition deficits: no recoveryafter extinction of overshadowing or blocking cues. Quart. J. Exp. Psychol. 52B(4), 307–333.

olland, P.C., Bouton, M.E., 1999. Hippocampus and context in classical conditioning.Curr. Opin. Neurobiol. 9 (2), 195–202.

guchi, Y., Fukumoto, K., Sawa, K., Ishii, K., 2014. Effects of extended context dis-crimination training and context extinction on transfer of context dependencyof conditioned flavor aversion. Behav. Process. 103, 218–227.

amin, L.J., 1969. Predictability, surprise, attention, and conditioning. In: Campbell,B.A., Church, R.M. (Eds.), Punishment. Appleton-Century-Crofts, New York, pp.

Please cite this article in press as: Carranza-Jasso, R., et al., Intertrialearning: Effects over the ABA renewal paradigm. Behav. Process. (201

279–296.asprow, W.J., Cacheiro, H., Balaz, M.A., Miller, R.R., 1982. Reminder-induced recov-

ery of associations to an overshadowed stimulus. Learn. Motiv. 13 (2), 155–166.aufman, M.A., Bolles, R.C., 1981. A nonassociative aspect of overshadowing. Bull.

Psychon. Soc. 18, 318–320.

PRESS Processes xxx (2014) xxx–xxx

Lovibond, P., Preston, G.C., Mackintosh, N.J., 1984. Contextual control of conditioningand latent inhibition. J. Exp. Psychol. Anim. Behav. Process. 10, 360–375.

Maren, S., Phan, K.L., Liberzon, I., 2013. The contextual brain: implications forfear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14 (6),417–428.

Matzel, L.D., Schachtman, T.R., Miller, R.R., 1985. Recovery of an overshadowed asso-ciation achieved by extinction of the overshadowing stimulus. Learn. Motiv. 16,398–412.

Miller, R.R., Barnet, R.C., Grahame, N.J., 1992. Responding to a conditioned stimulusdepends on the current associative status of other cues present during trainingof that specific stimulus. J. Exp. Psychol. Anim. Behav. Process. 18, 251–264.

Miller, R.R., Grahame, N.J., Hallam, S.C., 1988. Summation of responding to CSs andan excitatory test context. Anim. Learn. Behav. 18 (1), 29–34.

Miller, R.R., Matzel, L.D., 1988. The comparator hypothesis: a response rule for theexpression of associations. In: Bower, G.H. (Ed.), The Psychology of Learning andMotivation, vol. 22. Academic, Orlando, pp. 51–92.

Miller, R.R., Schachtman, T.R., 1985. The several roles of context at the time ofretrieval. In: Balsam, P.D., Tomie, A. (Eds.), Context and Learning. Erlbaum, Hills-dale, NJ, pp. 167–194.

Mustaca, A.E., Gabelli, F., Papini, M.R., Balsam, P., 1991. The effects of varying theinter-reinforcement interval on appetitive contextual conditioning. Anim. Learn.Behav. 19 (2), 125–138.

Nakajima, S., Tanaka, S., Urushihara, K., Imada, H., 2000. Renewal of extinguishedlever-press responses upon return to the training context. Learn. Motiv. 31,416–431.

Osborne, J.W., Overbay, A., 2004. The power of outliers (and why researchers shouldalways check for them). Pract. Assess. Res. Eval. 9 (6).

Pearce, J.M., 1987. A model for stimulus generalization in pavlovian conditioning.Psychol. Rev. 94 (1), 61–73.

Preston, G.C., Dickinson, A., Mackintosh, N.J., 1986. Contextual conditional discrim-inations. Q. J. Exp. Psychol. 38B, 217–237.

Rescorla, R.A., Durlach, P.J., 1987. The role of context in intertrial interval effects inautoshaping. Quart. J. Exp. Psychol. Sect. B 39 (1), 35–48.

Rescorla, R.A., Wagner, A.R., 1972. A theory of pavlovian conditioning: variationsin the effectiveness of reinforcement and nonreinforcement. In: Black, A.H.,Prokasy, W.F. (Eds.), Classical Conditioning II: Current Research and Theory.Appleton-Century-Crofts, New York, pp. 64–99.

Ricker, S.T., Bouton, M.E., 1996. Reacquisition following extinction in appetitiveconditioning. Anim. Learn. Behav. 24, 423–436.

Rosas, J.M., Bouton, M.E., 1998. Context change and retention interval have additive,rather than interactive, effects after taste aversion extinction. Psychon. Bull. Rev.5, 79–83.

Sunsay, C., Bouton, M.E., 2008. Analysis of a trial-spacing effect with relatively longintertrial intervals. Learn. Behav. 36 (2), 104–115.

Terrace, H.S., Gibbon, J., Farrell, L., Baldock, M.D., 1975. Temporal factors influencingthe acquisition and maintenance of an autoshaped keypeck. Anim. Learn. Behav.3 (1), 53–62.

Thomas, B.L., Larsen, N., Ayres, J.J.B., 2003. Role of context similarity in ABA, ABC, andAAB renewal paradigms: implications for theories of renewal and for treatinghuman phobias. Learn. Motiv. 34, 410–436.

Todd, T.P., Winterbauer, N.E., Bouton, M.E., 2012. Effects of the amount of acquisitionand contextual generalization on the renewal of instrumental behavior afterextinction. Learn. Behav. 40, 145–157.

Tomie, A., 1976. Interference with autoshaping by prior context conditioning. J. Exp.Psychol. Anim. Behav. Process. 2, 323–334.

Üngor, M., Lachnit, H., 2008. Dissociations among ABA, ABC, and AAB recoveryeffects. Learn. Motiv. 39, 181–195.

Urcelay, G.P., Miller, R.R., 2010. Two roles of the context in pavlovian fear condition-ing. J. Exp. Psychol. Anim. Behav. Process. 36 (2), 268–280.

Urcelay, G.P., Miller, R.R., 2014. The functions of contexts in associative learning.Behav. Process. 104, 2–12.

Urcelay, G.P., Witnauer, J.E., Miller, R.R., 2012. The dual role of the context in postpeakperformance decrements resulting from extended training. Learn. Behav. 40 (4),476–493.

Urushihara, K., Miller, R.R., 2009. Stimulus competition between a discrete cue and atraining context: cue competition does not result from the division of a limitedresource. J. Exp. Psychol. Anim. Behav. Process. 35 (2), 197–211.

Van Hamme, L.J., Wasserman, E.A., 1994. Cue competition in causality judgments:the role of nonpresentation of compound stimulus elements. Learn. Motiv. 25,127–151.

Wagner, A.R., 1981. SOP: a model of automatic memory processing in animal behav-

l intervals and contextual conditioning in appetitive pavlovian4), http://dx.doi.org/10.1016/j.beproc.2014.07.014

Welker, R.L., McAuley, K., 1978. Reductions in resistance to extinction and spon-taneous recovery as a function of changes in transportational and contextualstimuli. Anim. Learn. Behav. 6, 451–457.

1299

1300

1301