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The development of cued versus contextual conditioning in a predictable and an unpredictable human fear conditioning preparation Carlos Iberico a,b , Debora Vansteenwegen a, * ,1 , Bram Vervliet a,c , Trinette Dirikx a , Valerie Marescau a , Dirk Hermans a a Department of Psychology, University of Leuven, Belgium b Department of Psychology, Catholic University of Peru, Peru c Department of Psychology, University of Amsterdam, The Netherlands Received 8 January 2007; received in revised form 22 June 2007; accepted 4 August 2007 Available online 14 September 2007 Abstract In this human fear conditioning study, the online development of conditioned US-expectancy to discrete cues and background con- texts was measured in two groups. In the paired group (n = 30), the CS was systematically followed by an aversive shock (US). In the unpaired group (n = 30), CS and US were presented explicitly unpaired. Using US-expectancy ratings, we replicated the basic finding already illustrated in humans with startle modulation. In the paired group, the CS elicited more US-expectancy than the context, whereas in the unpaired group, the context elicited more US-expectancy than the CS. Interestingly, we also observed a trial-by-trial development of conditioning to the context in the unpaired group as indicated by a significant linear trend. This gradual development and the evidence for the role of US-expectancy in contextual fear add to the idea that cued and contextual fear rely on the same basic associative processes. Ó 2007 Elsevier B.V. All rights reserved. PsycINFO classification: 2343; 2360; 2560; 3211 Keywords: Contextual fear; US-expectancy; Human fear conditioning; Unpredictability; Startle modulation 1. Introduction Contemporary models of human classical conditioning in general, and of fear conditioning in particular, provide a rich conceptual framework for the understanding of the etiology, maintenance and treatment of human fears and phobias (Craske, Hermans, & Vansteenwegen, 2006; Mine- ka & Oehlberg, 2008). Based on new insights from both animal and human conditioning research that have accu- mulated over the last three decades, these contemporary models have been successful in addressing most of the crit- icisms that have been associated with old behaviouristic accounts of classical conditioning and of the acquisition of clinical fear (e.g., Mineka & Zinbarg, 2006; Mineka & Oehlberg, 2008). In a typical study, a neutral tone (condi- tioned stimulus; CS) is repeatedly presented together with an aversive electric shock (unconditioned stimulus; US). After a few trials, the originally neutral CS will start elicit- ing fear responses. At the learning level, an association is formed between the memory representation of the CS and the memory representation of the US. A number of animal neurobiological studies have focused on fear responses elicited by long-lasting stimuli such as enhanced startle responses by prolonged exposure to bright light in rats (Walker & Davis, 1997) or by admin- istration of corticotrophin-releasing hormone (Lee & Davis, 1997). Also increased freezing in a cage that has been associated with shocks, demonstrates fear to long- lasting contextual cues (e.g., Fanselow, 2000). Different 0001-6918/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.actpsy.2007.08.001 * Corresponding author. Address: Centre for the Psychology of Learn- ing and behaviour therapy, Department of Psychology, Tiensestraat 102, B-3000 leuven, Belgium. Tel.: +32 16 32 61 34. E-mail address: [email protected] (D. Vansteen- wegen). 1 Postdoctoral researcher of the fund for Scientific Research (Flanders). www.elsevier.com/locate/actpsy Available online at www.sciencedirect.com Acta Psychologica 127 (2008) 593–600

The development of cued versus contextual conditioning in a predictable and an unpredictable human fear conditioning preparation

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Available online at www.sciencedirect.com

www.elsevier.com/locate/actpsy

Acta Psychologica 127 (2008) 593–600

The development of cued versus contextual conditioning in apredictable and an unpredictable human fear conditioning preparation

Carlos Iberico a,b, Debora Vansteenwegen a,*,1, Bram Vervliet a,c, Trinette Dirikx a,Valerie Marescau a, Dirk Hermans a

a Department of Psychology, University of Leuven, Belgiumb Department of Psychology, Catholic University of Peru, Peru

c Department of Psychology, University of Amsterdam, The Netherlands

Received 8 January 2007; received in revised form 22 June 2007; accepted 4 August 2007Available online 14 September 2007

Abstract

In this human fear conditioning study, the online development of conditioned US-expectancy to discrete cues and background con-texts was measured in two groups. In the paired group (n = 30), the CS was systematically followed by an aversive shock (US). In theunpaired group (n = 30), CS and US were presented explicitly unpaired. Using US-expectancy ratings, we replicated the basic findingalready illustrated in humans with startle modulation. In the paired group, the CS elicited more US-expectancy than the context, whereasin the unpaired group, the context elicited more US-expectancy than the CS. Interestingly, we also observed a trial-by-trial developmentof conditioning to the context in the unpaired group as indicated by a significant linear trend. This gradual development and the evidencefor the role of US-expectancy in contextual fear add to the idea that cued and contextual fear rely on the same basic associative processes.� 2007 Elsevier B.V. All rights reserved.

PsycINFO classification: 2343; 2360; 2560; 3211

Keywords: Contextual fear; US-expectancy; Human fear conditioning; Unpredictability; Startle modulation

1. Introduction

Contemporary models of human classical conditioningin general, and of fear conditioning in particular, providea rich conceptual framework for the understanding of theetiology, maintenance and treatment of human fears andphobias (Craske, Hermans, & Vansteenwegen, 2006; Mine-ka & Oehlberg, 2008). Based on new insights from bothanimal and human conditioning research that have accu-mulated over the last three decades, these contemporarymodels have been successful in addressing most of the crit-

0001-6918/$ - see front matter � 2007 Elsevier B.V. All rights reserved.

doi:10.1016/j.actpsy.2007.08.001

* Corresponding author. Address: Centre for the Psychology of Learn-ing and behaviour therapy, Department of Psychology, Tiensestraat 102,B-3000 leuven, Belgium. Tel.: +32 16 32 61 34.

E-mail address: [email protected] (D. Vansteen-wegen).

1 Postdoctoral researcher of the fund for Scientific Research (Flanders).

icisms that have been associated with old behaviouristicaccounts of classical conditioning and of the acquisitionof clinical fear (e.g., Mineka & Zinbarg, 2006; Mineka &Oehlberg, 2008). In a typical study, a neutral tone (condi-tioned stimulus; CS) is repeatedly presented together withan aversive electric shock (unconditioned stimulus; US).After a few trials, the originally neutral CS will start elicit-ing fear responses. At the learning level, an association isformed between the memory representation of the CSand the memory representation of the US.

A number of animal neurobiological studies havefocused on fear responses elicited by long-lasting stimulisuch as enhanced startle responses by prolonged exposureto bright light in rats (Walker & Davis, 1997) or by admin-istration of corticotrophin-releasing hormone (Lee &Davis, 1997). Also increased freezing in a cage that hasbeen associated with shocks, demonstrates fear to long-lasting contextual cues (e.g., Fanselow, 2000). Different

594 C. Iberico et al. / Acta Psychologica 127 (2008) 593–600

neurobiological structures such as hippocampus and bednucleus of the stria terminalis (BNST) seem to be involvedin fear elicited by long lasting contextual stimuli and not infear elicited by specific short-duration cues such as a condi-tioned tone or light (Kim & Fanselow, 1992; Lee & Davis,1997; McNish, Gerwitz, & Davis, 1997; Philips & Ledoux,1992; Waddell, Morris, & Bouton, 2006).

This dissociation corresponds nicely with the clinicaldistinction between fear and anxiety (e.g., Bouton, Barlow,& Mineka, 2001; Lang, Davis, & Ohman, 2000; Quinn &Fanselow, 2006; Mineka & Oehlberg, 2008). Pathologicalfear is compared with reactions to an explicit discrete cuewith focused escape or avoidance as the outcome ofincreased cue proximity. In contrast, clinical anxiety isassociated with a more general form of distress elicitedby less specific cues, involving physiological arousal butwithout organized functional behaviour. In contrast to fearthat is obvious in patients with phobia or panic disorder,anxiety is characteristic of patients with generalized anxietydisorder. The latter shows an apprehensive anticipation offuture danger for which no specific cues are available.

It is surprising that despite these clinical and neurobio-logical interests contextual fear in humans has onlyreceived little attention. Nevertheless, Grillon and co-workers (e.g., Grillon, 2002b) developed a powerful para-digm using the baseline startle response as an index of fearelicited by a long-lasting stimulus (contextual fear), andstartle potentiated by specific cues as an index of cued fear.They showed that clinically anxious patients respond withsustained levels of anxiety to stressful contexts, but they donot show exaggerated fear responses to explicit cues (e.g.,Grillon, Morgan, Davis, & Southwick, 1998). In healthyparticipants, they (e.g., Grillon & Davis, 1997) createdtwo conditions: one group received unpaired shocks(unpredictable group); in the second group the shocks werealways preceded by a CS (predictable group). The unpre-dictable group showed larger baseline startle responsesthan the predictable group, indicating more anxiety elicitedby the experimental context. This is in line with the well-demonstrated negative effects of unpredictability anduncontrollability in ethological and clinical models (Bar-low, 2000; Mineka & Kihlstrom, 1978; see also Baas, vanOoijen, Goudriaan, & Kenemans, 2008).

A learning or conditioning account can explain this setof findings. Different stimuli such as the CSs and the con-text, compete to acquire associative strength. Tomie(1976), for example, showed in an autoshaping procedurewith pigeons that prior exposures to an unsignaled US,interferes with future conditioning with that US. This inter-ference only occurred when training and testing occurred inthe same context, and disappeared when the US was pre-dicted by another cue during preexposure. Supposedly,the US-preexposure trials resulted in an associationbetween the experimental context and the US, which thenblocked subsequent learning about the CS (for alternativeexplanations see Baker, Mercier, Gabel, & Baker, 1981).Similarly in the higher described unpredictable group, the

USs are actually contingent upon the presence of the exper-imental background context. As a consequence, the contextwill gain associative strength with the US and elicit expec-tancy of the US. In the predictable group, however, the CS-US pairings lead to fear elicited by the specific CS and littlefear will generalize to the context. In line with this, Vans-teenwegen, Iberico, Vervliet, Marescau, and Hermans(2007) demonstrated in a similar experiment that the con-text (a long-lasting stimulus) in the unpredictable conditiondoes indeed elicit US-expectancy. Allegedly, the chronicanticipation of threat mediates the sustained level of anxi-ety as measured by baseline startle responding. In learningterms, the difference between fear and anxiety can thereforebe defined as cued fear versus contextual fear.

Next to addressing the central role of US-expectancy,associative learning accounts such as the Rescorla–Wagnermodel (Rescorla & Wagner, 1972) are also very specific aboutthe development of learning on a trial-by-trial basis. In thecase of unpredictability in a fear conditioning experiment,for instance this model predicts that contextual fear willgradually develop over trials when the context gains associa-tive strength as the best predictor for shock. In the predict-able case, no differentiation would be predicted between theCS and the context in the beginning of acquisition butgradually the CS would gain more associative strength incomparison to the context. Hence from an associativeperspective, basic learning processes involved in cued condi-tioning and contextual learning are, although elicited bydifferent types of stimuli (a context and a cue), very similar.

In previous research on contextual fear in humans thedevelopment of contextual conditioning was never explic-itly investigated. First, in most experiments on contextualfear only baseline startle responding at the beginning of aseparate test session, for example one week later, wasreported (e.g., Ameli, Ip, & Grillon, 2001; Grillon & Davis,1997) and not intertrial interval responding (ITI) duringthe development of contextual conditioning. Second, inmost studies only startle modulation was used as an indexof conditioning. Usually startle modulation data are notreported on a trial-by-trial basis but instead blocks are usedbecause of the high levels of variability in the psychophys-iological response (Blumenthal et al., 2005).

The aim of the present study was to compare the onlinedevelopment of cued and contextual fear in a predictableand an unpredictable situation by including online US-expectancy ratings, next to the standard startle modula-tion. We collected US-expectancy ratings during the CSsand during the context (ITI responses). In our lab, we haveconducted several fear conditioning studies using onlineUS-expectancy measures as an index of learning (e.g. Vans-teenwegen et al., 2007; Vervliet, Vansteenwegen, Hermans,& Eelen, 2007). With regard to cued conditioning, thismeasure shows nice acquisition and extinction learningcurves. Hence the measure has the advantage of reflectingthe evolution of US-expectancy during the whole experi-ment (online) and can show the gradual development ofcued and contextual learning on a trial-by-trial basis. In

C. Iberico et al. / Acta Psychologica 127 (2008) 593–600 595

the present study, two groups were created: A paired groupand an unpaired group. In the paired group, one neutralvisual stimulus was immediately followed by shock (CS+)whereas the other visual stimulus was not (CS�). In theunpaired group, both visual stimuli were in 50% of the tri-als followed by a shock presented 8.5–11.5 s after CS-offset.It was expected that in the unpaired group contextual con-ditioning would develop gradually over trials as the contextacquires associative strength. In contrast no contextualconditioning would develop in the paired context, becausethe CS+ accurately predicts shock.

2. Method

2.1. Participants

Sixty first-year psychology students (9 males and 51females) with an average age of 19 (SD = 2.55) participatedin this study. They all gave informed consent and wereinstructed that they could decline to participate at any time.

3. Apparatus

3.1. Description of startle measurement

The startle probe that elicited the startle response was a100 dB burst of white noise with instantaneous rise timepresented binaurally for 50 ms through headphones. Theprobes were delivered every 12–25 s.

Orbicularis Oculi electromyographic activity (EMG)was recorded with three Ag/AgCl Sensormedics electrodes(0.25 cm diameter) filled with a TECA electrolyte. Aftercleaning the skin with peeling creme to reduce inter-elec-trode resistance, electrodes were placed on the left side ofthe face according to the site specifications proposed byFridlund and Cacioppo (1986). The raw signal was ampli-fied by a Coulbourn isolated bioamplifier with bandpass fil-ter (v75-04). The recording bandwidth of the EMG signalwas between 10 Hz and 20 kHz (±3 dB). The signal wasrectified online and smoothed by Coulbourn multifunctionintegrator (v76-23 A) with a time constant of 50 ms. In thestartle probe phases, signal measuring started 1 s beforenoise onset at 1000 Hz. From noise onset, the signal wasdigitized at 1000 Hz for 1000 ms.

3.2. Description of the expectancy online

The expectancy of the US (shock) was measured using acustom built dial operated by the participants’ right hand.The pointer was turned through 180� from 0 to 100, 0 indi-cated that the participant did not expect any shock at all,and 100 that the participant certainly expected the shock.

3.3. Description of SCR measurement

Electrodermal activity was recorded with Fukuda stan-dard Ag/AgCl electrodes (1 cm diameter) filled with KY

gel and attached to the hypothenar palm of the left hand,which was cleaned with tap water. The inter-electrode dis-tance was 2.5 cm. The Coulbourn skin conductance coupler(V71-23) provided a constant 0.5 V across the electrodes.The analogue signal was passed a 12-bit AD-converter anddigitized at 10 Hz during 16 s (from 2 s prior to conditionedstimulus onset until 6 s after the conditional stimulus offset).

3.4. Description of the US-shock

Electrocutaneous stimulation of 2 ms duration wasdelivered by surface Sensormedics electrodes (1 cm diame-ter) filled with a neutral gel and were attached to the rightwrist. The intensity was set at a level that the participanthad described as ‘‘unpleasant and demanding some effortto tolerate’’. The shock was delivered by a digitimer, a con-stant current stimulator. The digitimer stimulator modelDS7A provides constant current high voltage pulses ofbrief duration for percutaneous stimulation during investi-gation of the electrical activity of nerve and muscle tissue.The output current is continuously variable over the rangeof 0–100 milli-amps, from a source voltage continuouslyvariable from less than 100–400 V, to meet the require-ments of human pathological cases. The pulse width rangecan be up to 2 ms. A specially designed isolated outputstage maintains a square (current) pulse shape while mini-mizing stimulus artifacts.

3.5. Description of CSs

Two spider pictures selected from The InternationalAffective Picture System (IAPS) (Lang, Bradley, & Cuth-bert, 1999) were used as CS+ and CS� in both groups.The CSs were always presented for 8 s and the assignmentof the spider pictures to CS+ and CS� was counterbal-anced over participants within each group.

4. Procedure

The experiment consisted of one session with fourphases: a preparation phase, a startle habituation phase,a habituation phase and a conditioning phase.

4.1. Preparation phase

Before the session started, participants were informed(orally and written) that shocks and loud noises would bedelivered and that they should try to predict the deliveryof the shock using the expectancy online dial. They weretold that the shock could be presented before, during,and after the picture, and they should indicate their expec-tancy of the shock during the whole experiment, not onlyduring the presentation of the CS. After signing theinformed consent, participants went to the experimentalroom where electrodes were attached and the intensity levelof the shock/US was selected. The experimenter graduallyincreased the intensity of the shock until the participant

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reported that it was ‘‘unpleasant and demanding someeffort to tolerate’’.

4.2. Startle habituation phase

Four startle probes were presented within an interval of65 s.

4.3. Habituation phase

In this phase, a block of 2 CS+ and 2 CS� presentationswas given. Throughout the experiment, a trial consisted ofan 8 s presentation of the CS followed by an interstimulusinterval of on average 20 s. For each CS, during one trial astartle probe was presented during the CS (6 s after CS-onset) and during the other trial a probe was presentedduring the ITI-interval (8 s before the onset of the follow-ing CS). The order was counterbalanced.

4.4. Conditioning phase (acquisition)

In both groups two blocks of 8 CS+ and 8 CS� trialswere presented. In the paired group, the shock was admin-istered immediately after CS offset for three out of fourCS+ trials (75% partially reinforced). We decided to par-tially reinforce in order to delay the moment of contin-gency awareness because we were interested in thedevelopment of US-expectancy learning. In the unpairedgroup, the delivery of the shocks was explicitly unpaired,that is, the shocks were delivered in the absence of theCSs within the interstimulusintervals at two differentmoments (8.5 or 11.5 s after the offset of the CS). In addi-tion to this, in both groups (paired and unpaired) half ofthe startle probes were delivered during a CS (5 or 6 s afterCS onset) and the other half in absence of the CS (8 or 6 sbefore the CS onset). The presentation order of the differ-ent trialtypes within a block was random.

5. Response definition

5.1. Startle response

For all valid trials, peak amplitudes were defined as themaximum of the response curve within 21–175 ms after thestartle probe onset. Every peak amplitude was scored bysubtracting its baseline score (averaged EMG level between1 and 20 ms after the noise onset). Then, the raw scoreswere converted to z scores to neutralize the individual dif-ferences among the participants. Averages were calculatedfor the first half of acquisition and the second half of acqui-sition for responses during CS+, CS� and ITI separatelyfor the paired and the unpaired group.

5.2. US-expectancy

A/D units were registered by the computer and laterthese scores were converted back to the original values

between 0 and 100. Each trial was divided in 8 time inter-vals of 4 s for which we computed the mean. The mostimportant blocks are the fourth and the eighth block.US-expectancy ratings given between 4 and 8 s after CS-onset were averaged (fourth block) and considered asresponses to the cues. The eighth block was chosen to bean index of expectancy during intertrial intervals becausewithin this interval baseline responding to context alonecould be measured without interference of occasional US-presentations in the unpaired group.

5.3. Skin conductance

Skin conductance responses were measured because theywere taken in all our previous fear conditioning studies.However, the data will not be reported here as onlyresponses elicited by the CSs and not the contexts weremeasured.

6. Results

6.1. US-expectancy

In Fig. 1, mean US-expectancy ratings for CS+, CS�and ITI are represented for the paired and the unpairedgroup separately. The figure shows a nicely developingCS+/CS� differentiation in the paired group that is notpresent in the unpaired group. The ITI-expectancy ratingsshow over trials a clear increase in the unpaired group,which is absent in the paired group.

A Group (paired/unpaired) X Stimulus (CS+/CS-/ITI)X Trial ANOVA was conducted on the US-expectancy rat-ings. Apart from a significant main-effect of Stimulus, F(2,116) = 43.44, p < .001, MSE = 70639.1 and of Trial, F(15,870) = 2.31, p = .003, MSE = 14194.1, there was also a sig-nificant Stimulus X Trial interaction, F(30, 1740) = 3.66,p < .001, MSE = 7750.5 and most importantly a significantGroup X Stimulus X Trial interaction, F(30, 1740) = 4.84,p < .001, MSE = 7750.5.

The higher described observations with regard to cueconditioning were corroborated by specific statistical tests.Although no differences were obtained between CS+ andCS� at the first trial, there was a clear differential condi-tioning effect at the end of acquisition in the paired group,resulting in a significant CS+/CS� X linear trend over tri-als interaction F(1, 58) = 44.84, p < .0001, MSE = 20733.7.This interaction was absent in the unpaired group, F < 1.Moreover, when contrasting the difference in linear trendfor CS+ and CS� between the two groups a significantthree-way interaction was obtained, F(1, 58) = 22.23,p < .0001, MSE = 20733,7.

With regard to contextual conditioning, a significantlinear trend in ITI-responses over trials was observed inthe unpaired group, F(1, 58) = 17.04, p = .0001, MSE =24950.6 and no significant changes in the paired group,F(1, 58) < 1. The between group comparison of this effect

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Fig. 1. Trial-by-trial development of US-expectancy during CS+, CS� and ITI for the paired group and the unpaired group separately.

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was also significant, F(1, 58) = 16.22, p < .001,MSE = 24950.6.

When comparing the trend for ITI and CS+ in thepaired group over trials there was a significant interaction,F(1, 58) = 29.54, p < .0001, MSE = 21492.6, indicatingthat the increase in the CS+ was significantly larger thanin the ITI. In the unpaired group, the opposite patternwas observed, the linear increase was significantly largerfor the ITI than for the CS+, F(1, 58) = 10.36, p < .01,MSE = 21492.6. This resulted in a significant three-wayinteraction, F(1, 58) = 37.44, p < .0001,MSE = 21492.6.Finally, in the paired group, the CS� responses decreasedsignificantly over trials (linear trend for CS� over trialsF(1, 58) = 7.54, p < .01, MSE = 31089.9) but differed notsignificantly from the ITI changes over trials, F(1,58) = 2.29, p = .135, MSE = 12220.5. In the unpairedgroup, US-expectancy elicited by the CS- did not changeover time, F < 1 and a significant difference with theincreasing linear trend in ITI-responding was obtained,F(1, 58) = 18.54, p < .0001, MSE = 12220.5.

6.2. Startle modulation

In Fig. 2 mean startle responses for CS+, CS� and ITIprobes (averaged in blocks of four trials), are presented fortwo acquisition blocks separately for the paired and theunpaired group. The most prominent observation was thegeneral decrease in startle responding over the two blocksregardless of the type of stimulus.

A Group X Stimulus X Block ANOVA was conductedand revealed next to a significant main-effect of Stimulus,F(2, 116) = 21.49, p < .001, MSE = 0.175 also a strongeffect of Block, F(1, 58) = 29.03, p < .001, MSE = 0.369indicating a general decrease in startle responding over tri-als. No main-effect of group was obtained, F(1, 53) = 2.68,p = .11, MSE = 0.176. Most interestingly, the Group X

Stimulus X Block interaction was also significant, F(2,116) = 3.45, p = .035, MSE = 0.2147.

Although no differences were obtained between the twogroups for the CS+/CS� differentiation in the first block,F(1, 58) < 1. There was a clear difference in this differenti-ation between the two groups in the second acquisitionblock, F(1, 58) = 9.04, p < .01, MSE = 0.217. The expectedbetween group interaction was also significant, F(1,58) = 8.29, p < .01, MSE = 0.173.

For the paired group, the difference between CS+ andCS� at the end of acquisition was significant, F(1,58) = 15.34, p < .001, MSE = .217. For the unpaired groupit was not, F(1, 58) < 1. Looking at the means in Fig. 2, wecan conclude that only in the paired group responses to theCS+ stay high over conditioning trials and that all otherresponses decline.

With regard to contextual conditioning, a significantdecrease in responding was obtained in the paired group,F(1, 58) = 7.43, p < .01, MSE = 0.217. However also inthe unpaired group a significant decrease was obtained,F(1, 58) = 7.07, p = .01, MSE = .238 and the non-signifi-cant Group X Block interaction indicated that no signifi-cant differences in these decreases between groups werefound, F < 1. Obviously, the general decreasing tendencyin the startle data over blocks has played an important rolein these observations.

When comparing ITI and CS+ in the paired groupbetween the first and the second block of acquisition, therewas no significant interaction, F < 1, indicating no differ-ences in decrease over trials. However during the secondblock the difference between CS+ and ITI was significantF(1, 58) = 22.26, p < .001, MSE = 0.19. Between CS- andITI no significant difference in decrease was obtained,F < 1. In the unpaired group, also no significant differencesin decrease over blocks between the CS+, CS� and ITI(pairwise tested) were obtained.

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Fig. 2. Mean startle responses amplitudes (T-scores are used for graphic purposes) for CS+, CS� and ITI during the first and the second block ofacquisition for the paired and the unpaired group separately.

598 C. Iberico et al. / Acta Psychologica 127 (2008) 593–600

7. Discussion

The present study was set up to investigate the develop-ment of cued and contextual conditioning in a predictableand an unpredictable human fear conditioning preparationusing online US expectancy ratings. For the paired group,our data showed the development of conditioning to theCS+ and no conditioning to the context. In contrast inthe unpaired group, conditioning to the context graduallydeveloped over trials and no conditioning to CS+ orCS� occurred. The present data show that contextual con-ditioning results from the fact that in the absence of goodcue predictors, the contextual stimulus gradually gainsassociative strength. These findings add to the idea thatcontextual conditioning, just like cued learning, is basedon an associative learning process, most probably a trial-by-trial error correction mechanism.

Although the CS-over-context effect in the paired groupand the context-over-CS effect in the unpaired group ismore than once reported using startle modulation as anindex of learning (e.g., Ameli et al., 2001; Grillon & Davis,1997) this is the first time that these effects are demon-strated using US-expectancy ratings that show the develop-ment over learning trials in such a detail. The present datareveal additional information about what is happeningwithin the human fear conditioning sessions. It was clearlyillustrated that the context-over-CS effect in the unpairedgroup was the result of a linear increase of the US-expec-tancies during the context over trials and not of decreasingexpectancies during the CS. The CS-over-context effect inthe paired group was the result of increasing expectanciesduring the CS and not decreasing expectancies during thecontext. Some authors (see e.g., Grillon, 2002a; Odling-Smee, 1975) conceptualize fear conditioning as a processwhereby initial generalized fear of contextual stimulibecomes stimulus specific following the learning of danger

and safety cues. In the case of unpredictability fear wouldremain generalized. However, the present US-expectancydata do not seem to corroborate this idea: contextual con-ditioning was absent in the predictable situation whereas itgradually developed in the unpaired situation.

Another interesting observation is that contextual con-ditioning seems to develop more slowly than cued condi-tioning. This can be explained by a difference in saliencebetween the cues and the context. In the Rescorla–Wagnermodel (Rescorla & Wagner, 1972) the change in associativestrength on a given trial is not only determined by theamount of expectancy discrepancy but also by the salienceof the stimuli. Alternatively, it is also possible that in theunpaired group CS+ and CS� gained some associativestrength because they were both followed by the US in50% of the trials. The CSs may therefore have competedwith the context resulting in slower context conditioning.However, the long intervals between the offset of the CSand the onset of US in the unpaired group put this alterna-tive into question.

Unfortunately, we were not able to replicate the basiccontextual conditioning effect in our startle data. Both,the unpaired as well as the paired group showed a signifi-cant overall decrease in startle responding regardless ofthe type of stimulus. Only for the CS+ in the paired groupthe decrease was not significant. Hence, we did obtain evi-dence for cued fear learning in the paired group when com-paring with the unpaired group, but we did not obtaindifferences in contextual fear between the two groups. Itis not clear why we did not observe the contextual condi-tioning effect in this fear index although we did obtainthe effect in the US-expectancy ratings. Moreover, in awithin-subjects variant of this study, we did observe con-textual conditioning in startle (Vansteenwegen et al., 2007).

One possibility is that the general strong decline in startleresponding over trials might have made it more difficult to

C. Iberico et al. / Acta Psychologica 127 (2008) 593–600 599

observe differences in contextual fear. Possibly, an insuffi-cient number of startle habituation trials before the startof the acquisition phase was responsible for this decline.Second, we used a different method than in most reportedstudies. That is, we only looked at ITI-startle responses dur-ing the conditioning phase whereas most studies used abetween-session measurement and compared baseline star-tle at the beginning of a second session. Grillon (e.g.,2002a) even demonstrated that longer intervals betweenthe acquisition session and the test session revealed strongercontextual fear effects in startle. Hence, it is possible that thedemonstration of the contextual fear conditioning effect inbetween- a subject design is dependent on the method usedto calculate changes in contextual fear. A third possibility isthat the US used in this experiment was, although adequateto influence the US-expectancies, not strong enough to elicitreal levels of chronic fear/anxiety. A final possibility is thatthe addition of the US-expectancy online measure inter-fered with the measurement of the psychophysiologicalresponses or changed the nature of the conditioning task.However, this explanation does not hold as recently Vans-teenwegen et al. (2007) demonstrated the contextual condi-tioning effect in US-expectancy online and startle at thesame time. Further research should more systematicallyinvestigate the contextual fear conditioning effect using dif-ferent experimental designs and different indices of learning(see also Grillon, Baas, Cornwell, & Johnson, 2006).

In sum, the present study demonstrated human contex-tual conditioning due to unpaired presentations of the CSand the US using online US-expectancy ratings as indexof learning. Just like cued conditioning in the paired condi-tion, contextual conditioning develops gradually over trialsin the unpaired condition. When cued and contextual con-ditioning are used as an experimental model to study thedifferences in etiology and preconditions between fearand anxiety, one should keep in mind that they both seemto be based on the same basic associative process. Forexample, Grillon (2002a, 2002b) demonstrated that deficitsin cued fear learning resulted in more contextual fear andsuggested that deficits in cognitive skills and operationsimportant for associative learning were responsible for thiseffect. Based on the idea that similar associative processesunderlie cued and contextual fear, it is difficult to under-stand how associative learning deficits can be responsiblefor a deficit in cued fear learning but not in contextual fearlearning. Hence differences between fear and anxietyshould not be explained by factors related to associativeprocessing. Future research should focus more on differ-ences due to the typical characteristics of the stimuli (spe-cific discrete cues and long-lasting stimuli) and/or thetypical pattern of conditioned reactions elicited by fearand anxiety (Bouton et al., 2001; Quinn & Fanselow, 2006).

Acknowledgement

The authors would like to thank Anne Vandersmissenfor her assistance in running the experiment.

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