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1 Learning and Motivation 4 (29) Contents lists available at ScienceDirect Learning and Motivation journal homepage: Context blocking in rat autoshaping: Sign-tracking versus goal-tracking Daniel S.J. Costa, Robert A. Boakes * School of Psychology (A18), University of Sydney, NSW 26, Australia article info abstract Article history: Received 2 August 28 Revised November 28 Available online 16 December 28 Keywords: Context blocking Autoshaping Sign-tracking Goal-tracking Trace conditioning Rats Prior experience of unsignaled food can interfere with subsequent acquisition by birds of autoshaped key-pecking at a signal light. This has been understood to indicate that unsignaled food results in context conditioning, which blocks subsequent learning about the keylight food relationship. In the present experiment with rats lever insertion as the conditioned stimulus (CS) preceded sucrose delivery as the unconditioned stimulus (US). Half the rats initially received unsignaled USs in the conditioning context, while the remainder did not. Both lever-presses (sign-tracking) and magazine-entries (goal-tracking) were recorded. Under immediate reinforcement conditions, prior unsignaled US interfered with signtracking, but had no effect on goal-tracking. In two further groups, a trace condition prevented development of sign-tracking. In this case, prior context conditioning interfered with goal-tracking. These results suggest that interference with sign-tracking may reflect response competition, while interference with goal-tracking under trace conditions may reflect failure to acquire a CS US association. Ó 28 Elsevier Inc. All rights reserved. Contemporary analyses of classical conditioning propose that the pairing of a conditioned stimulus (CS) and an unconditioned stimulus (US) can result not only in the formation of associations between CS and US, but also between contextual cues and the US (Bouton, 27). Furthermore, the strength of the conditioned response appears to be inversely related to the strength of the context-us association (Balsam & Schwartz, 1981). One source of evidence is the US pre-exposure effect, in which prior to the arrangement of a classical contingency between a CS and a US, the US is first presented unsignaled in the conditioning context; such pre-exposure has been found to result in slower acquisition of respond- * Corresponding author. Fax: address: bobb@psych.usyd.edu.au (R. A. Boakes) /$ - see front matter Ó 28 Elsevier Inc. All rights reserved. doi:.16/j.lmot
2 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) ing to the CS (Baker, Mercier, Gabel, & Baker, 1981; Randich & LoLordo, 1979). In an early example of this effect involving autoshaping with pigeons, the delivery of unsignaled response-independent food prior to conditioning substantially retarded acquisition of pecking at the keylight, a phenomenon then labeled learned laziness (Engberg, Hansen, Welker, & Thomas, 1972). The contribution of context conditioning to this effect was indicated by Tomie s (1976) finding that extensive prior exposure to unsignaled food deliveries retarded the acquisition of autoshaped key-pecking only if the food was delivered in the same context as conditioning. Balsam and Schwartz (1981) obtained a similar result with ring doves and in addition found that both acquisition and maintenance of conditioned responding were inversely and monotonically related to the number of previous non-contingent food presentations. Pecking at the keylight, an example of sign-tracking, was the only response recorded by Engberg et al. (1972), Tomie (1976) and Balsam and Schwartz (1981). An alternative explanation to associative blocking for the effect of unsignaled USs on subsequent conditioning is that the context comes to control some form of conditioned behavior that competes with the development of sign-tracking when a localized CS is introduced. This response competition possibility was discussed by Balsam (198) who suggested that a context containing unsignaled USs comes to elicit general activity. In his experiments, this was measured in terms of movement across hinged panels comprising the floor of a conditioning chamber used for pigeons and doves. Although he did not report a US pre-exposure experiment using this measure, he did show that a keylight paired with food could come to elicit general activity under conditions that failed to produce key-pecking, namely, when the inter-trial interval was no longer than the keylight duration of 36 s (Balsam, 198; pp. 14 1). A more specific response than general activity that has been recorded in the course of autoshaping experiments is approach to the site of reinforcement following presentation of the CS, a phenomenon termed goal-tracking (Boakes, 1977). The occurrence of goal-tracking can indicate that animals have learned to associate a localized CS with the US, despite the absence of responding directed at the CS (sign-tracking). It is therefore possible that interference with sign-tracking produced by US preexposure results at least partly from response competition, as suggested by Balsam (198), but specifically from a change from sign- to goal-tracking in the way the CS US association is expressed. There have been at least two examples where goal-tracking measures have revealed learning about the predictive relationship between a localized CS and a US that did not result in sign-tracking. One example comes from experiments that have introduced a trace interval. Thus, in a pigeon autoshaping experiment in which unusually magazine-entries were recorded as well as keypecks, Brown, Hemmes, Cabeza de Vaca, and Pagano (1993) arranged that food followed the offset of a keylight by 6 s. The key-pecking that occurred with a zero trace failed to appear under these trace conditions. However, magazine-entries during the keylight CS developed as rapidly in the trace as in the zero trace condition. When a similar comparison was made in a rat autoshaping preparation of the kind used in the present experiment and with the same length of the trace period, s, Costa and Boakes (27) found, like Brown et al. (1993), that this trace effectively abolished sign-tracking in this case, lever-pressing but had no detectable effect on goal-tracking. These results suggest that at least under autoshaping conditions the introduction of trace intervals of this magnitude can have a greater effect on the nature of the conditioned response (CR) than on acquisition of the CS US association. It should be noted, however, that, when a sexual US was used in an autoshaping experiment using quail, introducing a trace interval reduced sign-tracking but did not produce goal-tracking (Burns & Domjan, 1996; Experiment 3). A second example in which goal-tracking and sign-tracking measures diverged comes from an experiment that gave rats repeated exposure to a light before it served as the CS in an autoshaping procedure. This pre-exposure retarded sign-tracking relative to a control group for which the light was novel thus appearing to produce a latent inhibition effect but had no detectable effect on the development of goal-tracking (Boughner & Papini, 23). In the light of the above examples it seemed possible that the effects of prior exposure to the US on the autoshaped behavior of rats might differ according to whether goal-tracking or sign-tracking is considered. The present experiment was designed to test this possibility. The preliminary aim was to establish whether in rats prior context conditioning would attenuate sign-tracking under zero trace (immediate reinforcement) conditions, as previously obtained in birds (e.g. Balsam & Schwartz, 1981).
3 18 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) The second aim was to determine whether prior context conditioning would attenuate magazine-entry as well as sign-tracking. We gave one group unsignaled food pellets in the conditioning context, i.e. context conditioning, prior to introducing an autoshaping procedure in which lever insertion signaled pellet delivery immediately after the lever retracted (Block-Immediate group) and compared this group to a group that had not been given food in the conditioning context prior to the autoshaping procedure (Control-Immediate). Confirmation of a US pre-exposure effect for sign-tracking would be shown by less lever pressing in the Block-Immediate than in the Control-Immediate group, while little difference in goal-tracking between the two groups would suggest that there was not an associative blocking effect. Following our previous finding that rats tend to goal-track rather than sign-track with a trace interval of s (Costa & Boakes, 27), the third aim of the experiment was to test whether prior context conditioning would affect acquisition of goal-tracking under trace conditions. Thus a further group (Block-Trace group) was given the same context conditioning as the Block-Immediate group prior to introduction of a trace autoshaping procedure in which pellet deliveries occurred s after the lever had been retracted. This group was compared to a control group (Control-Trace) that was not given context conditioning prior to the trace autoshaping. As neither group was predicted to display signtracking, our main interest was whether in this case context conditioning would block the development of goal-tracking. The lack of any indication of conditioned behavior in the Block-Trace group would be consistent with an associative blocking effect. As in any experiment involving such appetitive reinforcers, an initial phase was required in order to train rats to drink sucrose promptly from the dipper before lever-sucrose pairings were introduced. Given that such magazine training inevitably involves context conditioning, we followed Tomie (1976) by giving this training to all rats in an altered version of the conditioning context, achieved in the present case by manipulating visual, auditory, tactile and olfactory cues in the conditioning chambers with the aim of reducing to a minimum generalization from the altered to the normal context. Methods Subjects The experiment was run in two replications. At the start of the first, 14 female hooded Wistar rats were 212 days old, with a mean weight of 221 g, range g, and at the start of the second replication, 14 female hooded Wistar rats were 137 days old, with a mean weight of 213 g, range g. All animals had previously participated in an experiment in which they were exposed to different flavors and allowed to run in an activity wheel; they received no instrumental or classical training that resembled the present procedure. The rats were housed in the colony room in large acrylic tubs measuring cm, in groups of eight, although only seven from each tub were used in the experiment. Eight rats from the first replication were allocated to the two Trace conditions (each n = 4), while six were allocated to the Imm conditions (each n = 3). These numbers were reversed for the second replication, such that, after both replications, all groups comprised seven rats. They were maintained on a food deprivation schedule providing 2-h access to food each day following an experimental session. Apparatus Seven conditioning chambers (skinner boxes), measuring cm, were contained within sound and light attenuating wooden cabinets. These were each fitted with a ceiling-mounted 4 W houselight and a fan providing some masking noise, and both were switched on throughout every experimental session, except as noted below for the altered context. In each chamber the two end walls and ceiling were aluminum, the side walls were clear Plexiglas and the floor was composed of 16 stainless steel rods. A dipper could be used for deliveries of. ml of 2% sucrose in tap water into a magazine aperture located in the center of one end wall. The same wall contained two 48-mm
4 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) wide retractable levers (MED Instruments Inc.) on either side of the magazine aperture, but only the right-hand lever was used in this experiment. This lever was mounted such that, when extended, the lever projected 19 mm into the chamber, with its top surface 6 mm above the floor of the chamber. The distance from the left-hand edge of the lever to the center of the magazine aperture was 6 mm. An infrared sensor was fitted across the magazine aperture to allow recording of magazine-entries. For initial habituation and magazine training an altered context was created by lining the floor of each operant chamber with chicken mesh and placing an open jar of Vicks Vaporub above the chamber ceiling. s involving this altered context were run with houselight and fan switched off. Procedure All animals first received a -min habituation session in the altered context with a Petri dish containing ml of 2% sucrose solution. Three sessions of magazine training followed, each consisting of 2 sucrose deliveries on a VT 3-s schedule, also in the altered context. In the context conditioning phase, the conditioning chambers were returned to their normal state and remained unaltered for the rest of the experiment. With the levers retracted, rats in the Block-Imm and Block-Trace groups received 2 noncontingent deliveries of sucrose with a dipper time of -s on a variable 6-s (VT 6-s) schedule in each of two sessions. During these sessions, rats in the Ctrl-Imm and Ctrl-Trace groups were not given any sucrose but spent the same amount of time in the conditioning chambers as the other rats. In the subsequent classical conditioning phase, each session contained 2 trials, each trial commencing with -s insertion of the right-hand lever and concluding with response-independent delivery of sucrose (-s dipper time). A variable inter-trial interval of 6 s (VT 6-s) was used, where the inter-trial interval was defined as the period commencing with dipper-retraction in one trial and ending with lever insertion in the next trial. For subjects in groups Ctrl-Imm and Block-Imm, sucrose delivery followed immediately after lever-retraction, while for subjects in groups Ctrl-Trace and Block-Trace sucrose was delivered s after lever-retraction. Data analysis Since, as previously (e.g. Costa & Boakes, 27), lever-pressing rates followed a skewed distribution, the non-parametric Mann Whitney U-test was used to analyze group differences on this measure. On the other hand, since magazine-entry data were approximately normally distributed, parametric analyses were applied to the number of magazine-entries made during the s prior to lever insertion (Pre-CS), during the s of lever insertion (CS) and to CS pre-cs difference scores for each trial, calculated by subtracting pre-cs magazine-entries from CS entries and for trace conditions from entries during the -s trace interval. A 2 () mixed ANOVA applied to these data compared Blocked with Control condition as the between-group factor (separately for each trace condition) and trend over sessions as the within-subject factor. Results Sign-tracking As seen in Fig. 1, only group Ctrl-Imm acquired lever-pressing. By response rates in this group were reliably greater than those in the Block-Imm group, U(7, 7) = 9, p =.4, thus confirming that the context conditioning procedure had reduced sign-tracking. In the trace condition, only 2 rats out of 14 showed any tendency to press the lever (none of the other rats exceeded an average of 1. responses/min), and, as suggested by the right-hand panel of Fig. 1, there was no detectable difference in this response in between the Block-Trace and Ctrl-Trace groups, U(7, 7) = 7, p >.. Goal-tracking during lever insertion Magazine-entries during the s prior to lever insertion (pre-cs) and during lever insertion (CS) are shown in Fig. 2. A mixed ANOVA applied to these data from the Immediate groups (left-hand
5 182 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) Block-Imm Block-Trace Ctrl-Imm Ctrl-Trace Median lever-presses/min Fig. 1. Left-hand panel: median lever-press rates for the Block-Imm and Ctrl-Imm groups during zero trace conditioning whereby sucrose was delivered immediately following -s lever insertion. The groups differed in that only the Block-Imm group had received prior context conditioning. Right-hand panel: Median lever-press rates for the Block-Trace and Ctrl-Trace groups during trace conditioning whereby sucrose was delivered s after the lever was retracted. These groups also differed in that only the Block-Trace group had received prior context conditioning. panel) revealed that the difference between pre-cs and CS scores approached significance, F(1,12) = 3.79, p =.8, and, importantly, this difference interacted with, F(1,12) = 4.96, p =.2, The main effect of Group (Block vs Control) approached significance, F(1,12) = 4.3, p =.7, but neither the main effect of nor any interaction came close to significance, largest F = 1.8. A subsequent analysis of CS pre-cs difference scores for magazine-entries by the two Imme- Mean number of magazineentries per trial 1 Block-Imm CS Ctrl-Imm CS Block-Imm Pre-CS Ctrl-Imm Pre-CS 1 Block-Trace CS Ctrl-Trace CS Block-Trace Pre-CS Ctrl-Trace Pre-CS Fig. 2. Left-hand panel: mean (±SEM) number of magazine-entries in the -s pre-cs period (unfilled markers) and during the -s CS period when the lever was present (filled markers) for the Block-Imm and Ctrl-Imm groups. Right-hand panel: Mean (±SEM) number of magazine-entries in the -s pre-cs period (unfilled markers) and during the -s CS period (filled markers) for the Block-Trace and Ctrl-Trace groups.
6 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) Block-Trace Trace Ctrl-Trace Trace Block-Trace Pre-CS Ctrl-Trace Pre-CS Mean number of magazineentries per trial Fig. 3. Mean (±SEM) number of magazine-entries during the -s trace interval and in the -s pre-cs period for the Block- Trace and Ctrl-Trace groups. Note that the pre-cs data shown here are identical to those shown in the right-hand panel of Fig. 2. diate groups revealed a linear trend, F(1, 12) = 6.77, p =.23, but, as suggested by the left-hand panel of Fig. 2, no main effect of Group, F < 1, and no interaction between this factor and trend, F(1, 12) = 1.2, p >.. Thus, although at the start of training the Block-Immediate group tended to make more magazine-entries than the Control-Immediate group both before and during lever insertion, goal-tracking, as measured by CS pre-cs scores, was acquired by both groups at a comparable rate. As for the two Trace groups, analysis of the CS and pre-cs magazine-entries shown in the righthand panel of Fig. 2 revealed a significant linear trend over sessions, F(1, 12) = 6.76, p =.2, but no other main effects or interactions, largest F = Although inspection of these data suggested that the Ctrl-Trace, but not the Block-Trace, group developed some goal-tracking during the CS, analysis of CS pre-cs difference scores in the two trace groups did not reveal any main effect or interaction, largest F(1,12) = Goal-tracking during trace intervals The mean number of magazine-entries during the trace interval and during the s prior to lever insertion are illustrated in Fig. 3. The trace pre-cs difference score was subjected to a mixed ANOVA (Group ). These data could, of course, be collected only from the two trace groups, where the important result was a main effect of Group, F(1, 12) =.16, p =.4. Other than the suggestion of a quadratic trend, F(1,12) = 6.22; Bonferroni F crit = 6., there were no trends or interaction between Group and trend, largest F(1, 12) = Rats in Ctrl-Trace made more magazine-entries during the trace interval than in the -s preceding the CS, F(1,6) = 13.22, p =.1, while the number of magazine-entries made by rats in Block-Trace did not differ from pre-cs to trace, F < 1. Thus, there was no evidence even on this measure that the latter group had learned to associate the lever with sucrose delivery. Discussion The main result in terms of lever-pressing was to confirm for the rat autoshaping procedure the context blocking effect previously reported for pigeons (Tomie, 1976) and ring doves
7 184 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) (Balsam & Schwartz, 1981): previous unsignaled deliveries of sucrose in the conditioning context prevented the subsequent development of sign-tracking that was otherwise produced by pairing lever insertion with immediate sucrose delivery. Such blocking of sign-tracking was not found under - s trace conditions for the simple reason that, as previously found (Costa & Boakes, 27), sign-tracking did not develop under these conditions, even in the absence of prior context conditioning. The main new results from this experiment arose from recording magazine-entries in order to measure goal-tracking. For the groups given the immediate reinforcement condition, goal-tracking during lever insertion developed in a comparable way whether or not the rats had been given the context conditioning treatment, as seen in the left-hand panel of Fig. 2. Thus, although the sign-tracking results are consistent with those from previous context blocking studies, these goal-tracking results suggest that the acquisition of CS US associations under immediate reinforcement conditions was not detectably affected by prior US-only sessions. The marginal finding that early in conditioning Block rats given Immediate training (see Fig. 2, left-hand panel) showed a greater tendency than their Controls to enter the magazine both before and during lever insertion supports the proposal that context conditioning interferes with subsequent sign-tracking because it establishes a competing response rather than because of associative blocking (Balsam, 198). As noted in the Introduction, a similar response competition account has been proposed for a CS pre-exposure effect in an autoshaping experiment (Boughner & Papini, 23). More generally these findings provide further evidence that recording more than one kind of response can be important in classical conditioning experiments (cf. Holland, 1977, 198). A quite different pattern of results was seen in the groups given the trace condition. The control group not given prior context conditioning, Group Ctrl-Trace, showed some goal-tracking during the CS (Fig. 2) and even more during the trace interval (Fig. 3). On the other hand there was no indication of goal-tracking by Group Block-Trace during either the CS or the trace interval. The complete absence of both sign- and goal-tracking in this group suggests that these rats had failed to acquire a lever-sucrose association and thus that the difference between Group Block-Trace and Group Ctrl- Trace was the result of associative blocking by prior context conditioning. Although not the direct concern of this experiment, an obvious question posed by the lever-press data from this and our previous experiments (Costa & Boakes, 27) and by key-pecking data from a comparable pigeon experiment (Brown et al., 1993), is why the introduction of a trace interval can abolish sign-tracking. A possible answer comes from making the distinction between sign-tracking as approach to a stimulus that has acquired positive hedonic value and goal-tracking as an anticipatory response (cf. Konorski, 1967; Wagner & Brandon, 21) and by assuming that sign-tracking will occur only if hedonic conditioning of the signal CS is strong enough to compete successfully with goal-tracking. Recent evidence supporting this assumption comes from an analysis of individual differences in rat autoshaping: This revealed that for sign-trackers rats that pressed at a high rate a lever whose insertion signaled food lever insertion subsequently served as a more effective conditioned reinforcer of a novel instrumental response (nose-poking) than for goal-trackers, rats that were trained under identical conditions but that displayed a high rate of magazine-entry in the presence of the lever (Robinson & Flagel, in press). This approach suggests that immediate reinforcement makes the lever in the present case or the lit key in pigeon autoshaping sufficiently attractive or gives it sufficient incentive salience (Berridge, 21; Robinson & Flagel, in press) via strong hedonic conditioning to produce sign-tracking but that with a trace interval hedonic conditioning is weaker (cf. Mazur, 1997) so that goal-tracking becomes the dominant response to the CS. In addition to the above distinction between sign-tracking as a result of hedonic conditioning and goal-tracking as an anticipatory conditioned response, it should be noted that there are two fundamental asymmetries between these two types of response. First, a goal-tracking response (magazine-entry, in this case) can occur at any time during a conditioning session, while sign-tracking can only occur in the presence of the CS (the lever in the present case). Second, magazine-entry is necessary to obtain the US, while lever-pressing is not; thus, instrumental conditioning may play a role in the acquisition and maintenance of goal-tracking (Farwell & Ayres, 1979; Holland, 1977). Whether or not the above account is correct, the main conclusion to be drawn from this experiment is that prior context conditioning can affect the outcome of a subsequent autoshaping procedure in two ways. It can shift behavior from sign-tracking towards goal-tracking a performance effect, as
8 D.S.J. Costa, R.A. Boakes / Learning and Motivation 4 (29) seen here under immediate conditions and it can interfere with learning about the CS US relationship associative blocking, as appears to have taken place here under trace conditions. Acknowledgments This research was partly supported by an Australian Postgraduate Award to DSJC and by an Australian Research Council grant to RAB. We thank Geoff Hall and Justin Harris for their helpful comments on an earlier draft of this paper. References Baker, A. G., Mercier, P., Gabel, J., & Baker, P. A. (1981). Contextual conditioning and the US preexposure effect in conditioned fear. Journal of Experimental Psychology: Animal Behavior Processes, 7, Balsam, P. D. (198). The functions of the context in learning and performance. In P. D. Balsam & A. Tomie (Eds.), Context and learning (pp. 1 21). Hillsdale, NJ: Lawrence Erlbaum. Balsam, P. D., & Schwartz, A. L. (1981). Rapid contextual conditioning in autoshaping. Journal of Experimental Psychology: Animal Behavior Processes, 7, Berridge, K. C. (21). Reward learning: Reinforcement, incentives and expectations. In D. Medin (Ed.), The psychology of learning and motivation (pp ). New York: Academic Press. Boakes, R. A. (1977). Performance on learning to associate a stimulus with positive reinforcement. In H. Davis & H. M. B. Hurwitz (Eds.), Operant pavlovian interactions (pp. 67 1). Hillsdale, NJ: Erlbaum. Boughner, R. L., & Papini, M. R. (23). Appetitive latent inhibition in rats: Now you see it (sign tracking), now you don t (goal tracking). Learning & Behavior, 31, Bouton, M. E. (27). Learning and behavior: A contemporary synthesis. Sunderland, Mass: Sinauer Associates. Brown, B. L., Hemmes, N. S., Cabeza de Vaca, S., & Pagano, C. (1993). Sign and goal tracking during delay and trace autoshaping in pigeons. Animal Learning & Behavior, 21, Burns, M., & Domjan, M. (1996). Sign tracking versus goal tracking in the sexual conditioning of male Japanese quail (coturnix japonica). Journal of Experimental Psychology: Animal Behavior Processes, 22, Costa, D. S. J., & Boakes, R. A. (27). Maintenance of responding when reinforcement becomes delayed. Learning & Behavior, 3, 9. Engberg, L. A., Hansen, G., Welker, R. L., & Thomas, D. R. (1972). Acquisition of key-pecking via autoshaping as a function of prior experience: Learned laziness? Science, 178, 2 4. Farwell, B. J., & Ayres, J. J. B. (1979). Stimulus reinforcer and response reinforcer relations in the control of conditioned appetitive head poking ( goal tracking ) in rats. Learning and Motivation,, Holland, P. C. (1977). Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. Journal of Experimental Psychology: Animal Behavior Processes, 3, Holland, P. C. (198). The influence of visual stimulus characteristics on the form of Pavlovian appetitive conditioned responding in rats. Journal of Experimental Psychology: Animal Behavior Processes, 6, Konorski, J. (1967). Integrative activity of the brain. Chicago: University of Chicago Press. Mazur, J. E. (1997). Choice, delay, probability and conditioned reinforcement. Animal Learning & Behavior, 2, Randich, A., & LoLordo, V. M. (1979). Associative and non-associative theories of the US preexposure phenomenon: Implications for Pavlovian conditioning. Psychological Bulletin, 86, Robinson, T. E., Flagel, S. B. (in press). Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biological Psychiatry. Tomie, A. (1976). Interference with autoshaping by prior context conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 2(4), Wagner, A. R., & Brandon, S. E. (21). A componential theory of Pavlovian conditioning. In R. R. Mowrer & S. B. Klein (Eds.), Handbook of contemporary learning theories (pp ). Hillsdale, NJ: Lawrence Erlbaum.
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