Simultaneous conditioning demonstrated in second-order conditioning: Evidence for similar associative structure in forward and simultaneous conditioning

LEARNING

AND

MOTIVATION

22, 253-268 (1991)

Simultaneous Conditioning Demonstrated in Second-Order Conditioning: Evidence for Similar Associative Structure in Forward and Simultaneous Conditioning ROBERT C. BARNET,

H. MOORE ARNOLD,

AND RALPH R. MILLER

State University of New York at Binghamton A second-order conditioning procedure was used to evaluate the associative consequences of forward versus simultaneous pairings of the first-order CS and US with water-deprived rats as subjects in a conditioned Iick suppression task. In Phase 1, a tone was presented in a forward, simultaneous, or explicitly unpaired relationship to shock. In order to assesswhat was learned in Phase 1, all animals in Phase 2 were exposed to clicks in a forward relationship to the tone. In order to determine the mediational role of the tone in promoting conditioned responding to the clicks, in Phase 3 the first-order tone was extinguished for some animals and not extinguished for others. A test for conditioned lick suppression to the first-order tone found responding to be superior in the subjects that received the tone and shock in a forward arrangement relative to subjects that experienced the tone and shock in a simultaneous arrangement. However, a test for suppression to the second-order clicks revealed substantial and equal fear of the clicks in those groups which were exposed to either forward or simultaneous tone-shock pairings in Phase 1, followed in both cases by forward click-tone pairings in Phase 2. These results indicate that temporal contiguity is a sufficient condition for the establishment of an association; however, a forward temporal relationship between stimuli (e.g., clicks -+ tone) appears necessary for expression of the association appropriate for anticipation of the US. Phase 3 tone extinction did not attenuate the ability of the second-order clicks to control behavior in either the forward or simultaneous case, which suggests that a representation of the firs-order tone played no mediational role in behavior controlled by the second-order clicks. The structures of forward and simultaneous associations are compared. Q 1991 Academic Press. Inc.

Support of this research was provided by National Institute of Mental Health Grant 33881 and the SUNY-Binghamton Center for Cognitive and Psycholinguistic Sciences. Thanks are due to Louis Matzel for centrally contributing to the conceptual development of this research. We are also grateful to Nicholas Grahame, Steve Hallam, James Miller, and Stanley Scoblie for their critiquing an earlier version of this report and to an anonymous reviewer for his/her insightful comments and suggestions. Requests for reprints should he addressed to Ralph R. Miller, Department of Psychology, SUNY-Binghamton, Binghamton, NY 139026000. 253 0023-9690/91 $3.00 Copyright 0 1991 by Academic Press, Inc. All rights of reproduction in any form reserved.

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Contiguity is the common denominator of all theories of associative learning. The contiguity principle states that events which occur proximally in time are apt to be associated. However, the inferior responding usually observed following simultaneous pairings of the conditioned stimulus (CS) and unconditioned stimulus (US), relative to short-delay forward CS-US pairings, is problematic for the contiguity principle. Typically, CS-US pairings result in less conditioned responding to a CS if the CS and US are paired in a strictly simultaneous rather than a forward manner (e.g., Pavlov, 1927). Traditionally, the apparent failure of simultaneous conditioning procedures to promote learning has been reconciled with the contiguity principle by assuming that in order for acquisition to occur, the CS truce, as opposed to the CS itself, must be contiguous with the US presentation (e.g., Pavlov, 1927). However, this post hoc notion is unsatisfactory because it is not part of a theoretical framework that goes beyond the phenomenon that it explains. That is, there is no other corroborating behavioral phenomenon that provides evidence for such a process. A more recent explanation of the apparent relative weakness of simultaneous conditioning posits that for effective conditioned responding to occur the CS must bear a predictive relationship to the US (e.g., Egger & Miller, 1962; Mackintosh, 1983; Rescorla, 1972). In this latter framework, a CS presented simultaneously with a US is assumed to result in no learning because it provides no predictive information about the impending occurrence of the US. However, there is considerable disagreement about the necessity of predictive information for the establishment of an association. For example, Logan (1977) has claimed that contiguity is a sufficient condition for learning within a variety of conditioning preparations in which the CS is not informative, including backward conditioning (i.e., US + CS), which like simultaneous conditioning often does not result in appreciable conditioned excitatory responding. Supporting this position, Burkhardt and Ayres (1978), Dolan, Shishimi, and Wagner (1985), Heth (1976)) and Mahoney and Ayres (1976) have all reported successful backward excitatory conditioning given appropriate conditions. Similarly, under select circumstances successful demonstrations of conditioning among simultaneously presented CSs and USs have also been reported (e.g., Heth, 1976; Heth & Rescorla, 1973; Mahoney & Ayres, 1976; Matzel, Castillo, & Miller, 1988a; Matzel, Held, & Miller, 1988b). These instances of backward and simultaneous conditioning are problematic for the view that predictive information is essential for learning to occur. Recently, two additional explanations have been offered as to why little conditioned responding is ordinarily observed after a CS is simultaneously paired with a US. Both endorse the importance of contiguity, but they offer different reasons for the weak responding to the CS that is ordinarily seen after simultaneous CS-US pairings. The first, which we will call the

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distraction hypothesis, was proposed by Rescorla (1980), and the second, which we will call the temporal coding hypothesis, was proposed by Matzel et al. (1988b). The distraction hypothesis argues that, in contrast to forward pairings, simultaneous pairings of two stimuli may result in the more salient stimulus distracting the animal from processing the alternate stimulus. When distraction was equated among low saliency stimuli that were paired either in a forward or simultaneous manner in Phase 1 of a sensory preconditioning experiment, and one of these stimuli was paired with the US in a forward manner in Phase 2, Rescorla found that simultaneous presentation of two low saliency cues resulted in an association that was stronger than that produced with forward pairings in the sensory preconditioning phase. In this view, a highly salient stimulus, such as a US, that is simultaneously presented with a CS distracts the animal from processing that CS; hence, no association is formed. On the other hand, Matzel et al. (1988b), like Logan (1977), argue that contiguity is sufficient for the establishment of an association. Matzel et al. argue that the frequently observed failure of simultaneous conditioning procedures to promote conditioned responding reflects a failure in the sensitivity of testing preparations to tap into the appropriate response system, rather than a failure in the acquisition or formation of a simultaneous association. Within this framework, “an association is formed between a simultaneously presented CS and US, but the CS does not evoke an anticipatory response (e.g., eyeblink, salivation, or suppression of ongoing behavior) because it does not bear a forward relationship to the US” (p. 319). This model posits that associations include not only simple associative links between events but also code information about the temporal relationship of the events. The temporal coding hypothesis accounts for Rescorla’s (1980) observations as well as Matzel et al. ‘s finding of associative learning about a CS and a US that are simultaneously paired. In Rescorla’s procedure, for example, a critical simultaneous conditioning group received a simultaneous tone-light compound immediately followed by white noise in Phase 1. The tone was then forward paired with the US in Phase 2. A test for simultaneous conditioning given by separate presentations of the light evidenced substantial excitatory responding. The temporal coding hypothesis readily accounts for these findings by assuming that the establishment of the tone-US association in Phase 2 was antedated by the formation of a simultaneous association between the light and tone in Phase 1. Presumably, test presentations of the light activated a representation of the tone, which anticipated presentation of the US; hence, anticipatory responding to the light was observed. In Matzel et d’s procedure, a click train was paired with a tone in a forward manner during Phase 1 (i.e., clicks + tone) of a sensory preconditioning experiment, and then during Phase 2 the tone and footshock were either forward

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paired or simultaneous paired. Thus, following Phase 2 the click train was temporally predictive of the putatively excitatory tone, and consequently expected to elicit anticipatory responding. A subsequent test for conditioned fear of the clicks revealed substantial and equal fear among both simultaneously and forward paired groups of animals relative to unpaired control animals, thereby indicating the formation of a strong CS-US association within both forward and simultaneous first-order conditioning preparations. This finding that an animal can learn about a CS which was simultaneously paired with a US is inconsistent with Rescorla’s notion that a US presented simultaneously with a CS may distract the animal from the CS, thereby rendering it less likely to enter into an association with the US. At present, the generality of this temporal coding hypothesis has not been tested beyond Matzel et al.3 (1988b) sensory preconditioning preparation. Here we report a parallel study using the second-order conditioning procedure. Moreover, complementing Matzel et al., and also Rizley and Rescorla (1972) who examined the effects of extinguishing the first-order Sl in both forward sensory preconditioning and forward secondorder conditioning, the present research contributes to a data base for comparing the associative structures resulting from both forward-paired and simultaneous-paired events. In the typical second-order conditioning experiment, the first-order stimulus (Sl) is forward paired with the US during Phase 1 (i.e., Sl + US), and then the second-order stimulus (S2) is forward paired with Sl during Phase 2 (i.e., S2 --+ Sl). During the test phase, S2 is presented alone, and second-order conditioning is observed when the magnitude of conditioned responding to S2 is large relative to the responding to S2 seen in some control group (e.g., a group for which Sl and US are presented unpaired during Phase 1). What mechanisms might underlie the phenomenon of second-order conditioning are of great theoretical interest, because S2 comes to elicit a conditioned response but has never itself been directly paired with the US. Central to the aims of the present experiment, Rizley and Rescorla (1972) point out that there are several possibilities for the associative structure which might mediate responding to S2 in standard second-order conditioning. Figure 1 illustrates four such possibilities (based in part on the discussion by Rizley & Rescorla, 1972). First, if Sl in Phase 1 comes to reliably elicit a CR, then the CR would also be elicited during Phase 2 in the presence of S2. To the extent that S2 and the CR occur together, this might afford formation of a direct S2-CR association (see Linkage a in Fig. 1). The formation of this association would obviously depend upon the ability of Sl to elicit the CR prior to the S2-Sl pairings. Second, the S2-Sl pairings during Phase 2 training could result in the establishment of an S2-Sl association. Following Phase 1, Sl elicits the CR, and S2

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-

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CONDITIONING

0us +

CR

(b)

CR

(c)

CR

(d)

FIG. 1. Four possible associative linkages which might underlie responding to the secondorder stimulus in second-order conditioning. S2, presentation of the second-order stimulus; S2 in circle, representation of S2, Sl in circle, representation of Sl; US in circle, representation of the unconditioned stimulus; CR, conditioned response.

comes to elicit the CR by virtue of this S2-Sl association (see Linkage b in Fig. 1). In this association, S2 responding is dependent upon the continued ability of Sl to elicit the CR. Third, an S2-Sl association might be formed because of the pairings of these stimuli during Phase 2, but the CR is predicated on activation of the US representation by Sl (see Linkage c in Fig. 1). This linkage is the most complex of those considered here, because S2 responding is dependent upon the sustained integrity of both the S2-Sl association (formed during Phase 2) and the Sl-US association (formed during Phase 1). Finally, a fourth mediator of responding to S2 could be in an association between S2 and the US (see Linkage d in Fig. 1). If in Phase 1 training Sl comes to reliably activate a US representation, then this representation would also be activated during Phase 2 in the presence of S2. To the extent that S2 and the US representation occur together, establishment of an S2-US association might be achieved. In this association, S2 responding would depend only on the ability of Sl to activate the US representation prior to S2-Sl pairings. It is important to note the similarity of Linkages b and c. Both of these linkages posit an association between S2 and Sl. More critical to the present experiment is that for both of these linkages, elicitation of the CR by S2 is dependent upon the continued ability of Sl to elicit the CR (whether by direct association to the CR or by association to the US). That is, S2 elicits a CR only because Sl continues to do so (cf. Rizley & Rescorla, 1972). One prediction arising from this view is that manipulations which degrade the ability of Sl to elicit the CR following the establishment of second-order conditioning, such as Sl extinction, should also degrade the efficacy of S2 in eliciting conditioned responding. If, on the other hand, S2-Sl associations are not part of the behavioral linkage by which S2 acts as a second-order CS, extinction of Sl should have no effect. Our experiment used a second-order conditioning paradigm in order

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TABLE 1 Paradigm” Group

Phase 1

Phase 2

FF FF/T SF SF/T SS UF

T+ + T+ + T+ T+ T+ T/ +

C+T C+T C+T C-T CT C-+T

Phase 3 TT-

Test C C C, C. C, C.

T T T T ‘IT

’ F, forward; S, simultaneous; U, unpaired; T, tone; + , footshock; T- , tone extinction; C, clicks; T+, tone-US simultaneous; +, followed by. Phases 1, 2, and 3 occurred in Context Train. Testing occurred in Context Test.

to examine learning about simultaneously presented first-order stimuli. Table 1 illustrates the paradigm. In Phase 1 Groups FF and FF/Treceived a first-order CS (i.e., tone) and footshock forward paired, whereas Groups SF, SF/T-, and SS received the tone and the footshock simultaneously paired and Group UF received them unpaired. In Phase 2, all subjects received the second-order CS (i.e., click train) forward paired with the tone except for Group SS for which the clicks and tone were simultaneous paired. This concluded training for most of the subjects. However, in Phase 3 Groups FF/Tand SF/Thad the tone extinguished in order to assessthe mediational role of the tone in the associative structure underlying any conditioned responding that might be seen to the clicks. At test, responding (conditioned lick suppression) to the clicks and the tone was observed separately.

METHOD Subjects Eighteen male and eighteen female, naive, Sprague-Dawley-descended rats obtained from our own breeding colony served as subjects. They were assigned to one of six groups (n = 6) counterbalanced for sex. Body weights ranged from 320 to 475 g for males and from 220 to 305 g for females. The animals were housed in standard hanging stainless-steel wiremesh cages in a vivarium maintained on a 16-h/8-h light/dark cycle, with experimental manipulations occurring near the middle portion of the light phase. The animals were allowed free access to food, while water availability was limited to 10 min/day following a progressive deprivation schedule imposed 6 days prior to the start of the study. From the time of weaning until the start of the study, all animals were handled for 30 s, three times per week.

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Apparatus Two types of enclosures were used. Enclosure Y was a clear, Plexiglas chamber in the shape of a box 22.75 x 8.25 x 13.0 cm (1 x w x h) with a floor constructed of 0.48-cm-diameter rods 1.5 cm center-to-center, shorted via NE-2 neons, which allowed constant-current footshock to be delivered by means of a high voltage AC circuit in series with a l.OMohm resistor. Each of six copies of Enclosure Y had its own environmental isolation chest. Enclosure Y was dimly illuminated by a 2-W incandescent house light mounted on an inside wall of the environmental isolation chest approximately 30 cm from the animal enclosure. Background noise, mostly from a ventilation fan, was 74 dB(C). Enclosure Z was a 25.5-cm-long box in a truncated-V shape (28 cm high, 21 cm wide at the top, and 5.25 cm wide at the bottom). Each of six copies of Enclosure Z had its own environmental isolation chest. The floor and sides of Enclosure Z were constructed of sheet metal. The ceiling was clear Plexiglas. The floor consisted of two parallel metal plates each of which was 2 cm wide with a 1.25-cm gap between them. Enclosure Z was dimly illuminated by a 7-W incandescent house light mounted on an inside wall of the environmental isolation chest approximately 30 cm from the animal enclosure with the light entering the animal enclosure primarily through reflection from the roof of the environmental chest. Background noise, mostly from a ventilation fan, was 74 dB(C). Throughout all phases of the experiment, Enclosures Y and Z were each equipped with a water-filled lick tube which extended about 1 cm into a cylindrical niche which was 4.5 cm in diameter, left-right centered with its bottom 1.75 cm above the floor of the apparatus, and 5.0 cm deep. An infrared photo emitter and detector was mounted 1 cm in front of the tip of the lick tube such that an animal had to break the light beam in order to drink. Two 10 x lo-cm square, 45-Ohm speakers were mounted on the rear and right interior walls of each chamber. One speaker could deliver a complex tone (3000 and 3200 Hz) 8 dB(C) above the ambient background noise of 74 dB(C). This complex tone, rather than a pure tone, was employed in order to lessen the differences in amplitude between resonances and dead spots. A second speaker could present a 6-s click train (BRS AU-902 audio generator) 8 dB(C) above background noise. A speaker on the wall of the experimental room provided constant white noise 8 dB(C) above the room’s 74 dB(C) background level which was employed in order to prevent auditory stimulus (click or tone) leakage between animal enclosures. Procedure The critical aspects of the procedure are summarized in Table 1. Acclimation training. On Days 1 and 3, all animals received one 30-

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min session/day in Context Train, which for half the animals in each group was Enclosure Y and for the remaining animals was Enclosure Z. On Day 2, all animals received one 60-min session in Context Test, which was the alternate enclosure (Z or Y) from that used as Context Train. These sessions allowed the animals to acclimate to Contexts Train and Test and to establish baseline rates of licking from the water tube. Latencies to lick for a first and second 5 cumulative s were recorded on each day for all subjects. First-order conditioning (Phase I). On Day 4, Group FF (forwardforward) and Group FF/T - (forward-forward with tone extinction) were exposed in Context Train to four presentations of a 5-s tone which terminated with the onset of a 5-s, 0.5-mA footshock. These pairings occurred within a single 60-min session in which pairings were initiated 10, 20, 37, and 50 min into the session. Group SF (simultaneous-forward), Group SF/T(simultaneous-forward with tone extinction), and Group SS (simultaneous-simultaneous) were exposed to four simultaneous presentations of the complex tone and the footshock. For these groups, onset and offset of the tone and footshock coincided. These simultaneous trials were distributed in the same manner as the forward pairings of Groups FF and FF/T - . Group UF (unpaired-forward) received the same number of tone and footshock presentations, but these stimuli were explicitly unpaired, with footshocks occurring at 6, 22, 39, and 51 min into the session, and tones occurring at 11, 16, 34, and 56 min into the session. Second-order conditioning (Phase 2). On Day 5, Group FF, Group FF/T- , Group SF, Group SF/T-, and Group UF were exposed in Context Train to four 5-s presentations of a click CS, each of which terminated with the onset of a 5-s presentation of the complex tone. These pairings occurred within a single 60-min session in which the pairings were initiated 10, 20, 37, and 50 min into the session. Group SS received the same number of click and tone pairings initiated at the same times within the session, but the click and tone presentations were simultaneous rather than serial. Tone extinction (Phase 3). During 60-min sessions in Context Train on Days 6 and 7, animals in Groups FF/Tand Group SF/Treceived 24 tone alone presentations per day for a total of 48 nonreinforced tone presentations in this phase. These nonreinforced tone presentations were designed to extinguish any conditioned fear accrued to the tone as a result of Phase 1 treatment. The tone presentations were pseudorandomly distributed throughout the extinction session. Animals in all other groups were placed in the conditioning chambers for comparable periods with no nominal stimulus being presented. Tone presentations were 5 s each in duration. Recovery. One 60-min recovery session was conducted on Day 8 and was designed to reestablish a stable rate of licking. During this recovery

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2.5

SF

SF/T-

A

FFIT-

SS

U=

GROUP FIG. 2. Mean latency to lick for 5 cumulative seconds in the presence of the secondorder click CS as a function of treatment group. Brackets represent standard errors.

session, all animals were placed in Context Test without any discrete stimulus being presented. Testing. On Day 9, all animals were tested for suppression of ongoing water tube licking in the presence of the clicks (i.e., the second-order CS), and on Day 10 suppression was tested in the presence of the tone ( i.e., the first-order CS). Testing consisted of placing each animal in Context Test and allowing it to complete 10 cumulative seconds of licking. At the completion of the initial 5 s of licking, the appropriate test stimulus was presented and the latency to complete an additional 5 s of licking in the presence of that CS was recorded. Latencies to complete a first and second 5 s of licking on Days 9 and 10 were transformed to log latencies in order to permit the use of parametric statistics. RESULTS Control by the Second-Order Clicks

One animal in Group SS died during the study. Mean latencies in log seconds to complete 5 cumulative seconds of licking in the presence of the clicks as a function or treatment condition are illustrated in Fig. 2. A single-factor analysis of variance on the click suppression data revealed a significant effect of treatment, F(5, 29) = 11.00, p < .OOl. Planned comparisons indicated that Groups FF and SF each suppressed to the clicks more than either of the control groups, Groups SS and UF, Fs(1, 29) 3 10.04, ps < .Ol. Group SF and Group FF did not differ from each

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2.5 G 8 =

2.0

t z

1.5

4 5

1.0

ii 0.5 SF

SF/T-

R

FFIT-

SS

LF

GROUP FIG. 3. Mean latency to lick for 5 cumulative seconds in the presence of the first-order tone CS as a function of treatment group. Brackets represent standard errors.

other, nor did the control groups (SS and UF) differ from each other, all ps > .lO. Control by the First-Order Tone

Mean latencies in log seconds to complete 5 cumulative seconds of licking in the presence of the tone as a function of treatment condition are illustrated in Fig. 3. A single-factor analysis of variance on the tone suppression data revealed a significant effect of treatment, F(5, 29) = 9.80, p < .OOl. Planned comparisons indicated that Group FF suppressed appreciably more to the tone than did Group SF, SS, or UF, Fs(1, 29) 2 11.21, ps < .Ol. Effect of First-Order Tone Extinction

Group FF/Tsuppressed significantly less to the tone than Group FF (see Fig. 3) indicating that tone extinction treatment did attenuate the ability of the tone to suppress ongoing licking, F(l, 29) = 18.75, p < .OOl. Attentuation of suppression to the tone as a result of extinction treatment was not seen in tone-shock simultaneously conditioned animals; that is, Groups SF and SF/Tdid not differ from each other, p > .25 (see Fig. 3), presumably because of a behavioral floor effect for simultaneous first-order conditioning. Of focal interest, tone extinction treatment did not attenuate the ability of the clicks to suppress ongoing licking. That is, planned comparisons between Groups SF and SF/Tand between Groups FF and FF/T - were nonsignificant, ps > . 10 (see Fig. 2).

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DISCUSSION The findings of the present experiment indicate that simultaneous pairings of a first-order CS and an aversive US can be as effective as forward first-order CS-US pairings in establishing a second-order CS with substantial excitatory response potential, provided that the second-order CS bears a forward relationship to the first-order CS. Presumably, in order to be an effective promoter of conditioned responding, a second-order CS must come to have a forward relationship with the US. This can be achieved either through a forward relationship between the first-order CS or, in the case and the US (i.e., traditional second-order conditioning) in which the first-order CS and the US are simultaneous, through a forward relationship between the second-order CS and the first-order CS (the present procedure). This is supported by the present findings which show that the animals which were exposed to simultaneous tone-shock pairings during Phase 1 and then exposed to forward click-tone pairings during Phase 2 (i.e., Group SF) exhibited substantial fear of the second-order clicks equivalent to that displayed by animals which were exposed to forward pairings of events in both phases of training (i.e., Group FF). When the first-order tone was unpaired with footshock (i.e., Group UF), or when the second-order click did not bear a forward relationship to the tone during Phase 2 (i.e., Group SS), little conditioned lick suppression to the clicks was observed. In contrast to the second-order conditioning data, the conventional simultaneous conditioning deficit was observed when the first-order tone was tested for its ability to suppress ongoing behavior (i.e., Group SF vs. Group FF). A tone previously paired in a simultaneous manner with a footshock US evoked significantly less conditioned responding than a tone previously paired in a forward manner with footshock. Thus, the present findings replicate the frequently observed inferiority of responding to simultaneously conditioned stimuli relative to forward conditioned stimuli. However, the equal responding seen to the secondorder clicks indicates that the deficit in responding to the tone seen in the animals which in Phase 1 experienced the tone and shock simultaneously, relative to the animals which experienced the tone and shock serially, was due to a failure to express an acquired association rather than a failure to acquire an association. This comparable responding to the clicks in Groups SF and FF is inconsistent with the distraction hypothesis because suppression scores to the second-order CS (i.e., clicks) indicate that Group SF acquired a tone-shock association in Phase 1 (latent with respect to lick suppression), whereas the distraction hypothesis states that the simultaneous US should have interfered with learning about the tone. However, the data are congruent with the temporal coding hypothesis, which posits equal (or superior) learning of simultaneous

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events relative to serial events, but with the encoding of different temporal information. The sensory preconditioning data of Matzel et al. (1988b) and the present data both support the view that classical conditioning conforms to the contiguity principle, with robust learning occurring with simultaneous events. Moreover, learning in forward, simultaneous, and backward cases appears to include information about the temporal relationship of the events, which is reflected in the differential first-order responding observed in these three situations. That is, different temporal relationships apparently engage different response systems, each appropriate for its particular temporal relationship between the CS and US. That organisms can abstract, code, and retain temporal relationships between stimuli has been both well investigated and acknowledged (e.g., Gibbon & Church, 1984; Meek & Church, 1983; Spetch & Wilkie, 1983). In fact, it has been demonstrated that rats are sensitive not only to the directionality of associates but also to the specific quantitative temporal relationship among differentially spaced, forward paired CSs and USs (e.g., Davis, Schlesinger, & Sorenson, 1989). Therefore, as posited by Matzel et al. (1988b), there is corroborating evidence that animals encode the temporal relationship that obtains among proximal events. The present findings also provide some insight into the underlying associative structure which mediates responding to the second-order CS. Post-training extinction of the first-order CS (i.e., tone), which was conditioned to the US through simultaneous pairings, did not attenuate the potential of the second-order CS (i.e., clicks) to control behavior. This was seen using the same training parameters and extinction treatment which Matzel et al. (1988b) found did attenuate responding to the secondorder CS within the sensory preconditioning paradigm. Matzel et al.3 success with first-order CS extinction treatment using the same parameters as we used suggests that our procedure would have detected any existing dependency of responding to the second-order CS mediated by the associative status of the first-order CS. The present observations are consistent with Rizley and Rescorla’s (1972) findings. They observed that post-training extinction of the first-order CS, which was conditioned to the US through forward pairings, did not attenuate the potential of the second-order CS to control behavior (but see Rashotte, Griffin, & Sisk, 1977). An associative linkage which depended on the representation of the first-order CS mediating responding to the second-order CS would cause extinction of the first-order CS to attenuate responding to the second-order CS. The present data replicate the finding of Rizley and Rescorla for conditioning with forward paired elements and extend the finding to conditioning with simultaneous paired elements. That is, with neither simultaneous nor forward conditioning of the first-order CS-US association does the first-order stimulus appear to play an important mediational

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role in the responding observed to a second-order stimulus within the context of second-order conditioned suppression. Two of the four associative linkages outlined earlier did require an S2Sl association, suggesting the importance of the associative status of Sl (see Linkages b and c in Fig. 1). The present data, as well as the data of Rizley and Rescorla (1972), do not support the view that this type of linkage plays an operative mediational role in second-order conditioned suppression. Thus, two possible associative mediators for the responding seen in second-order conditioning remain. One involves a direct association between S2 and the CR (see Linkage a in Fig. l), and the other involves an association between S2 and the US (see Linkage d in Fig. 1). The task at hand then is to discriminate between these two alternatives. Rizley and Rescorla’s (1972) data do not afford such a discrimination. The present data, however, could be viewed as disfavoring the S-R account of secondorder conditioning, which posits a direct S2-CR association. The S-R account (see Linkage a in Fig. 1) posits that the conditioned response elicited by Sl comes to be associated with S2 in the second-order conditioning phase (Phase 2), and, therefore, that the formation of this S2CR association depends upon the efficacy of Sl to elicit a CR prior to S2-Sl pairings. This account is quite plausible in the standard secondorder conditioning experiment because forward pairings of Sl and the US engender Sl with the capacity to elicit strong CRs. However, the present experiment deviated from typical second-order conditioning in that Sl, after Phase 1 simultaneous pairings with the US, did not reliably elicit strong conditioned responding (see Group SF in Fig. 3). Rather, Sl elicited only weak conditioned responding, and, therefore, a weak CR should have become conditioned to S2. That S2 responding was strong following simultaneous Sl-US pairings (indeed, as strong as when they followed forward Sl-US pairings) would argue against the formation of an S2CR association. The remaining associative structure involves an association between S2 and the US (see Linkage d in Fig. 1). The formation of this association in Phase 2 depends only on the ability of Sl to activate the US representation as a result of Phase 1 Sl-US pairings, and not the ability of Sl to elicit a response. Presumably, simultaneous (and forward) pairings of Sl and the US result in the establishment of an association between these elements during Phase 1. During Phase 2, activation of the US representation by Sl is anticipated by presentation of S2. It is this anticipatory relationship between S2 and the US representation which likely permits S2 to control anticipatory conditioned responding. Once it is created by S2-Sl pairings, the integrity of this S2-US association in principle could be sustained despite later modification of the associative status of Sl (e.g.,

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extinction). This would allow S2 to continue to elicit anticipatory CRs despite extinction of Sl. Independent of the underlying associative linkage, the present observations clearly suggest an equivalency of associative structure in secondorder conditioning that does not depend on whether the first-order CSUS pairings were forward or simultaneous. On the one hand, this conclusion must be qualified because it rests on a null result; that is, no effect on responding to the second-order CS was seen as a result of extinguishing the first-order CS. On the other hand, the decreased responding to the first-order CS observed as a result of extinction of that stimulus (see Group FF/T - in Fig. 3) suggests that the present experiment was sensitive to any potential effect on responding to the second-order CS of our extinction of the first-order CS. The efficacy of the tone extinction phase in reducing conditioned fear of the tone was only evidenced for animals exposed to forward CS-US pairings (i.e., Group FF/Trelative to Group FF). No attenuation of conditioned responding to the tone was observed in the behavior of animals exposed to simultaneous CS-US pairings (i.e., Group SF/Trelative to Group SF), although already low levels of responding in Group SF suggest that this was an artifact of the anticipatory response measure used (i.e., functionally a floor effect). The present results indicate that second-order conditioning indexed by conditioned suppression, although dependent upon the associative strength of the first-order CS during Phase 2, does not subsequently depend on the first-order CS. That is, an Sl-US association is necessary for the acquisition of a response to S2, but it does not mediate responding to S2 after acquisition. This finding for Phase 1 simultaneous associations in second-order conditioning is entirely consistent with Rizely and Rescorla’s (1972; also see Holland & Rescorla, 1975; Rescorla, 1982) finding concerning Phase 1 forward associations in second-order conditioning. Moreover, both outcomes contrast with data generated with the sensory preconditioning paradigm. In sensory preconditioning, post-training extinction of the Sl-US association that mediated acquisition of the higherorder association to S2 appears to degrade responding to the higher-order elements in both forward (Matzel et al., 1988b; Rizley & Rescorla, 1972) and simultaneous (Matzel et al., 1988b) cases. In addition to the parallels between the underlying associative structures of forward and simultaneous conditioning seen in second-order conditioning and sensory preconditioning, there is further evidence of parallel structures provided by post-training US inflation. Matzel et al. (1988b) and Sherman (1978) found that, following either forward or simultaneous first-order conditioning, unsignaled inflation of the US enhanced conditioned responding to the CS. This suggests a CS + US + CR linkage for both forward and simultaneous first-order conditioning.

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9, 14-30. Received February 19, 1990 Revised June 18, 1990