RETRACTED: Biological significance and posttraining changes in conditioned responding

Learning and Motivation 34 (2003) 303–324 www.elsevier.com/locate/l&m

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Biological significance and posttraining changes in conditioned respondingq

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Hern an I. Savastano and Ralph R. Miller*

Department of Psychology, State University of New York-Binghamton, Binghamton, NY 13902-6000, USA Received 10 December 2002; received in revised form 20 February 2003

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Abstract

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Increases in conditioned responding to a target stimulus achieved through posttraining extinction of a former companion stimulus (deflation) have proven moderately easy to obtain. In contrast, reductions in responding to a target as a result of posttraining pairings of its companion with the outcome (inflation) have proven more elusive. It has been suggested that stimuli with high biological significance (i.e., high response potential) are partially protected against inflation-mediated reductions in responding. Three conditioned suppression studies with rats systematically compared the consequences of posttraining inflation and deflation of companion stimuli. Experiment 1 replicated the previously observed asymmetries. Experiment 2 showed that inflation and deflation effects are symmetrical when target stimuli are of relatively low biological significance during training. Experiment 3 suggested that a biologically significant stimulus is also protected against reductions in its potential to act as an effective comparator stimulus. These findings challenge many contemporary theories of associative learning, particularly those designed to account for retrospective revaluation. Ó 2003 Elsevier Science (USA). All rights reserved.

An important empirical discovery in the study of associative learning was that behavioral control by the target conditioned stimulus (CS) can be influenced by posttraining changes in the associative status of a companion stimulus (one that was

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Support for the preparation of this manuscript was provided by NIMH Grants 11704-02 and 33881. We thank Francisco Arcediano, Raymond Chang, Daniel Choi, Martha Escobar, John Genua, Jennifer Kelschenbach, and Steven Stout for their comments on an earlier version of the manuscript. * Corresponding author. Fax: 1-607-777-4890. E-mail address: [email protected] (R.R. Miller). 0023-9690/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0023-9690(03)00012-2

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present when the target CS was being trained). For example, Kaufman and Bolles (1981) first presented rats with overshadowing treatment, in which a target CS was paired with an outcome (often an unconditioned stimulus [US]) in the presence of a more salient companion stimulus. This treatment typically yields less conditioned responding to the target CS than in a group in which the target CS was trained alone. Following training, Kaufman and Bolles extinguished (i.e., associatively deflated) the companion (overshadowing) stimulus and observed a vigorous response to the target CS at test (i.e., a ‘‘recovery’’ from the overshadowing deficit). The observation that conditioned responding could be altered in the absence of further training with the target CS challenged prevailing associative theories, which had commonly equated responding to the target CS (i.e., performance) with associative strength (learning; e.g., Rescorla & Wagner, 1972). Such observations inspired theories that focused on the comparison at test of associative strengths (or ÔexpectanciesÕ) as a determinant of response strength (e.g., Gallistel & Gibbon, 2000; Miller & Matzel, 1988). Representative of models that emphasize response rules for the expression of Pavlovian associations is the Ôcomparator hypothesisÕ (Miller & Matzel, 1988; Miller & Schachtman, 1985). According to this view, conditioned responding to the target CS depends on the strength of the target CS-outcome association relative to the associative strength of other punctate or contextual stimuli that were present during training, the so-called ‘‘comparator stimuli.’’ Fig. 1 depicts the comparator hypothesis with the outcome represented by a US. Three associative links are presumed to control responding: (a) the target CS–US association (Link 1), (b) the association between the target CS and its comparator stimulus (Link 2), and (c) the association between the comparator stimulus and the US (Link 3). At test, presentation of the target CS directly activates a representation of the US (through Link 1), which is compared to a representation of the US that is indirectly evoked through the sequen-

Fig. 1. The original comparator hypothesis. Arrows represent: (1) the target CS–US association, (2) the target CS–comparator stimulus within-compound association, and (3) the comparator stimulus–US association. At test, presentation of the target CS evokes two representation of the US, one directly (through Link 1) and another indirectly mediated through a representation of the comparator stimulus (Links 2 and 3). The strengths of the directly and indirectly activated US representations are compared to determine responding to the target CS.

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tial activation of a representation of the comparator stimulus (Link 2) and that comparator stimulusÕ association with the US (Link 3). Excitatory conditioning is presumed to be directly related to the strength of the CS–US association (Link 1) and inversely related to the product of the strengths of the CS–comparator association (Link 2) and the comparator–US association (Link 3). Importantly, the comparator hypothesis predicts that posttraining changes in the associative strength of a companion stimulus should influence responding to the target CS. For example, posttraining deflation (i.e., extinction) of the comparator stimulus should enhance responding to the target CS by reducing activation of the indirectly evoked US representation (as in Kaufman & Bolles, 1981). Conversely, posttraining inflation of the comparator stimulus, through additional pairings with the US, should reduce responding to the target CS by enhancing the indirectly activated US representation. The effects of posttraining deflation have been largely confirmed with a variety of procedures, tasks, and species. For example, Dickinson and Charnock (1985) reported alleviation of cue competition in rats through posttraining extinction of the overshadowing stimulus in instrumental responding; Kaufman and Bolles (1981) and Matzel, Schachtman, and Miller (1985) in Pavlovian overshadowing with rats; Wasserman and Berglan (1998) in overshadowing of causal judgment by humans; Blaisdell, Gunther, and Miller (1999) in Pavlovian blocking with rats; Arcediano, Escobar, and Matute (2001) in Pavlovian blocking with humans; Cole, Barnet, and Miller (1995) in the relative stimulus validity effect with rats; Blaisdell, Denniston, and Miller (2001) in the overexpectation effect with rats; Best, Dunn, Batson, Meachum, and Nash (1985), Kasprow, Schachtman, and Miller (1987), and Lysle and Fowler (1985) in Pavlovian conditioned inhibition with rats; Miller, Hallam, Hong, and Dufore (1991) in differential conditioned inhibition with rats; and Schachtman, Brown, Gordon, Catterson, and Miller (1987) in negative contingency conditioned inhibition with rats (however, like many effects it is clearly parametrically delimited as indicated by some failures to obtain this effect, e.g., Holland, 1999; Rauhut, McPhee, DiPietro, & Ayres, 2000). The effectiveness of posttraining inflation of the comparator stimulus (i.e., comparator stimulus–US pairings) has been more difficult to observe. Numerous attempts to induce a decrement in the conditioned response to the target CS by inflating its comparator stimulus have failed (Grahame, Barnet, & Miller, 1992; Larkin, Aitken, & Dickinson, 1998; Miller, Hallam, & Grahame, 1990). One potential explanation for the apparent asymmetry in the effects of posttraining inflation and deflation is provided by the comparator hypothesis. Posttraining deflation of the comparator stimulus operationally consists of presenting the comparator stimulus by itself, which might be expected to effectively weaken the CS–comparator stimulus association (Link 2, see Fig. 1) as well as the comparator stimulus–US association (Link 3). This would greatly diminish the product of Links 2 and 3, thereby enhancing the direct activation of the US representation and responding to the CS. In contrast, posttraining inflation of the comparator stimulus–US association through additional comparator stimulus–US presentations should increase the strength of Link 3, but simultaneously reduce the effective strength of Link 2 (as a result of the comparator stimulus being presented in the absence of the target CS). Therefore,

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in the framework of the comparator hypothesis much of the potential enhancement of the indirectly activated US representation as a consequence of strengthening Link 3 might be expected to be compensated for by reductions in the strength of Link 2. Whether decreased or increased responding to the target CS will be observed will presumably depend upon the relative increases and decreases, respectively, in the strengths of Links 3 and/or 2. Although this weakening-of-Link-2 account may contribute to the relative difficulty of obtaining posttraining inflation effects, it cannot be the whole story because inflation effects are readily obtained when target training and subsequent inflation targetÕs comparator stimulus are embedded in a sensory preconditioning procedure (e.g., Miller & Matute, 1996). In a sensory preconditioning procedure, a relatively neutral stimulus acts as the outcome for the target cue during the sensory preconditioning training, and is later made biologically significant through pairings of it with a US following posttraining inflation of the comparator stimulus. Importantly, when cue competition is embedded within a sensory preconditioning procedure, the target cue (assuming that it does not have inherent biological significance because it itself is a US due for example to its high intensity) does not acquire biological significance until the neutral outcome stimulus with which it is paired is paired with an actual US. Thus, following sensory preconditioning treatment a target cue still has little biological significance to protect it from decrements in its effective associative linkage to the outcome due to posttraining (i.e., postsensory preconditioning training) inflation of the target cueÕs comparator stimulus. Toward accounting for this ease of obtaining posttraining inflation effects in sensory preconditioning (in contrast to first-order conditioning) as well as the differential effectiveness of posttraining inflation and deflation procedures in first-order conditioning, Denniston, Miller, and Matute (1996) and Miller and Matute (1996) have stepped outside of the framework of the comparator hypothesis and suggested that animals behave in a fundamentally conservative way; once they have learned a biologically significant relationship within their environment, they are resistant to surrender it. Specifically, they proposed Ôbiologically significantÕ stimuli are protected against losing behavioral control as a consequence of posttraining inflation of their companion stimuli (Denniston et al., 1996; Miller & Matute, 1996). A biologically significant stimulus is here defined as one that controls behavior, either inherently (e.g., food, water, painful or intense stimulation, or sex), or through association with another biologically significant event (e.g., a CS that has been paired with an inherently biologically significant stimulus). This view is congruent with an earlier literature in which cue competition was found to decrease with the biological significance of the target cue (e.g., Feldman, 1975; Koksal, Domjan, & Weisman, 1994; LoLordo, Jacobs, & Foree, 1982). One example of associative inflation being modulated by the biological significance of the target CS is backward blocking. Backward blocking is procedurally identical to forward blocking except that the phases of training are reversed. In a backward blocking procedure, a compound consisting of two stimuli is reinforced in Phase 1 (i.e., AX–US), followed by reinforcement of one of the elements in Phase 2 (i.e., A–US). The phenomenon consists of weaker responding to CS X than if CS A was not associatively inflated in Phase 2. Backward blocking has generally been more

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easily demonstrated in studies involving human participants (Chapman, 1991; Shanks, 1985; Van Hamme & Wasserman, 1994; Wasserman & Berglan, 1998; Williams, Sagness, & McPhee, 1994; but see Larkin et al., 1998), than in studies using nonhuman subjects (e.g., Miller et al., 1990; Schweitzer & Green, 1982). One possible explanation for the greater ease in demonstrating backward blocking in human participants relative to nonhuman subjects is the biological significance of the outcomes used during training. That is, studies with humans typically use outcomes of low biological significance, for example causal attribution with respect to fictitious allergic reactions to foods experienced by hypothetical patients, whereas studies involving nonhuman subjects typically use biologically significant outcomes such as electric shock or food USs. However, when the backward blocking studies with nonhuman subjects used outcomes of low biological significance, backward blocking was observed (Denniston et al., 1996; Miller & Matute, 1996). The efficacies of posttraining inflation and deflation manipulations have been assessed separately across various procedures, tasks, and species. Whereas deflation effects are observed across a variety of situations, the efficacy of inflation appears to be limited to situations in which the target CS is of relatively low biological significance during training (i.e., does not elicit any sort of vigorous responding at any time prior to the posttraining inflation treatment [before or during the cue competition treatment], as when the training and inflation treatments are embedded in Phase 1 of sensory preconditioning treatment). The purpose of the present studies was to systematically compare the magnitude of inflation and deflation effects while equating the biological significance of the target CSs and keeping constant the procedure, task, and species. This consistency of conditions should facilitate comparisons of inflation and deflation effects against common baseline controls within a single experiment. In all experiments, we used a conditioned suppression paradigm with water-deprived rats as subjects. The CSs were various auditory stimuli, and the US was a brief, mild footshock. Conditioned responding was measured as the potential of a CS to suppress the ratsÕ ongoing operant lever-pressing for water reinforcement.

Experiment 1

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One possible account of the failure of prior attempts to obtain inflation effects in situations in which the target CS was biologically significant during training is that extremely high levels of conditioned responding in the control conditions may have permitted a ceiling effect to mask any effect of inflating the so-called comparator stimulus. In Experiment 1, we compared the magnitude of posttraining inflation and deflation in first-order conditioning, a situation in which the target CSs acquire biological significance prior to the time of revaluation training (see Table 1). All subjects received interspersed overshadowing-treatment pairings of two compound stimuli with the footshock US (AX–US/BY–US, with A and B more salient than X and Y) in Phase 1. In Phase 2, one overshadowing stimulus (A) was either associatively deflated (i.e., extinguished) or inflated (i.e., given further pairings alone with the US), and the number of Phase 2 trials was manipulated between groups (Low and High)

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Table 1 Design summary of Experiment 1 Group

Phase 1

Phase 2

Phase 3

Test

Low deflation High deflation Low inflation High inflation

AX–US/BY–US AX–US/BY–US AX–US/BY–US AX–US/BY–US

16 64 16 64

S– S– S– S–

X? X? X? X?

A– A– A–US A–US

Y? Y? Y? Y?

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Note. Group names denote the amount (High vs. Low) of Phase 2 posttraining revaluation (inflation or deflation) treatment of the overshadowing stimulus (A). CSs A and B were a white noise and a buzzing stimulus, counterbalanced within groups and more salient than target CSs X and Y; CSs X and Y were a click train and a tone, counterbalanced within groups. The US was a mild footshock. ÔSÕ was a flashing light stimulus that served as an outcome (a surrogate US) in Experiment 2; it had no direct relevance to Experiment 1 and was included only to increase the equivalence between experiments. Trials on either side of Ô/Õ were interspersed within each session. Ô–Õ denotes nonreinforcement.

Method

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because prior research had found that number of revaluation trials was a critical variable (e.g., Blaisdell et al., 1999); at least in rats large numbers of revaluation trials appear to be necessary to obtain significant changes in responding to the target cue. Within each group, responding to target CS X could be compared to responding to target CS Y as a control for stimulus specificity. In order to avoid scaling constraints, stimulus parameters were carefully selected to generate a moderate level of responding to Y in all groups.

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Subjects Subjects were 24 male and 24 female, young adult, experimentally naive, Sprague– Dawley descended rats obtained from our breeding colony. Body-weight ranges were 235–345 g for males and 175–235 g for females. Subjects were randomly assigned to one of four groups (ns ¼ 12), counterbalanced within groups for sex. The animals were individually housed in standard hanging stainless-steel wire-mesh cages in a vivarium maintained on a 16/8-h light/dark cycle, with experimental manipulations occurring near the middle portion of the light phase. The animals were allowed free access to food, whereas water availability was limited to 10 min per day following a progressive deprivation schedule initiated one week 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. Apparatus The apparatus consisted of 12 operant chambers each measuring 30:5 cm  27:5 cm  27:3 cm (l  w  h). All chambers had clear Plexiglas ceilings and side walls, and metal front and back walls. On one metal wall of each chamber, there was an operant lever and adjacent to it a niche (4:5  4:0  4:5 cm) centered 3.3 cm above the floor through the bottom of which a 0.04-cc cup could deliver water. Chamber floors were 4-mm stainless-steel grids spaced 1.7 cm apart center-to-center, connected with NE-2 neon bulbs, which allowed constant-current footshock to be

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delivered by means of a high-voltage AC circuit in series with a 1.0-MX resistor. All chambers were housed in sound and light attenuating environmental chests. Three 45-X speakers mounted on three different interior walls of each environmental chest could deliver a complex tone (consisting of 1000- and 1067-Hz pure tones), a 6 per s click train, and a white noise. Additionally, a buzzer mounted on each environment chest could deliver a buzzing sound. The tone, click, noise, and buzzer were produced at 9, 4, 22, and 26 dB, respectively, above the ambient background sound of 70 dB (A scale) that was produced primarily by a ventilation fan. An overhead flashing light stimulus was provided by a 60-W (nominal at 120 VAC) incandescent bulb driven at 100 VAC. Each chamber was dimly illuminated by a (#1820) houselight located behind the front wall of the chamber. Each subject was treated and tested exclusively in one chamber. Specific chamber assignments were counterbalanced among the four groups.

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Procedure Acclimation and shaping. On Days 1–5, acclimation to the experimental context and shaping of bar-press behavior were conducted during daily 60-min sessions. Subjects were shaped to bar press for water on a variable-interval 20-s schedule in the following manner. On Day 1, a fixed-time 2-min schedule of noncontingent dipper operation was concurrent with a continuous reinforcement schedule. On Day 2, noncontingent reinforcers were discontinued, and subjects were trained on the continuous reinforcement schedule alone. Next, a variable interval 20-s schedule was imposed and maintained until each animal had made at least 50 bar-presses in a session (Days 3–4). This schedule of reinforcement prevailed throughout the remainder of the experiment including testing. On Day 5, all animals received separate exposure to each of the stimulus elements with the intention of minimizing configural conditioning. Toward this end, two 60-s presentations of each auditory stimulus alone (tone, click, buzzer, and white noise) were scheduled on Day 5. Phase 1 (Overshadowing training). On Days 6 and 7, all groups received daily 60min sessions of overshadowing training with two compound CSs (AX and BY). The compound CSs were forward-paired with a 0.5-s, 0.50-mA footshock US (AX–US/BY–US). Two trials with each compound CS were interspersed among intertrial intervals of 12  4 min (measured from trial termination to trial onset), and trial orders were counterbalanced within groups. All CSs were 60 s in duration. The onset of the footshock US coincided with the termination of the CSs. The tone and click served as target CSs X and Y, counterbalanced within groups. The white noise and buzzer served as the overshadowing CSs A and B, counterbalanced within groups. Phase 2 (Revaluation). On Days 8–11, subjects received either inflation or deflation of the overshadowing stimulus A. Deflation groups received either 16 (4/day; Low Def) or 64 (16/day; High Def) 60-s presentations of A-alone. Inflation groups either received 16 (4/day; Low Inf) or 64 (16/day; High Inf) pairings of A with the footshock US (A–US). Intertrial intervals were 5  2 min. Durations of these daily sessions were 80 min for the High groups and 20 min for Low groups.

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Results and discussion

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Phase 3 (Dummy exposure to S). On Days 12 and 13, all subjects were exposed to a flashing light stimulus to equate experience with the light with the animals in Experiment 2, which used the flashing light as a surrogate outcome within a sensory preconditioning procedure. Four nonreinforced presentations of the 5-s flashing light were scheduled per day within a 60-min session, separated by intertrial intervals of 12  4 min. Restabilization. On Days 14 and 15, daily 60-min sessions to restabilize baseline bar-pressing on the variable interval 20-s schedule were administered. After two such days, all subjects were bar-pressing at least 50 times per hour. Testing. On Day 16, the potential of the target stimuli to suppress baseline barpressing was assessed. In a 30-min session, all subjects received two nonreinforced presentations of each target stimulus, X and Y, separated by a 7-min intertrial interval. Trial orders were counterbalanced within groups. There were two schedules: X, Y, Y, X and Y, X, X, Y. All subjects failing to make at least 50 bar-presses in the test session were eliminated from the experiment. The number of bar-presses emitted during the 120 s immediately prior to presentation of each CS and in the presence of each 60-s CS were both recorded. For each subject, a suppression ratio for each CS was calculated to assess conditioned suppression. The suppression ratio consisted of the total number of bar presses made during both of each CSÕs presentations divided by the sum of that number plus half the total number of bar-presses made during the 120-s intervals that immediately preceded each 60-s CS (i.e., BPcs =ðBPcs þ 0:5BPprecs Þ). An a level of .05 was established for all statistical tests.

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A one-way analysis of variance (ANOVA) of baseline lever-press rates during the last session of restabilization revealed no main effect of Group, p > :50. Baseline response rates at this time (one day prior to the start of testing) were 21.04, 27.50, 24.38, and 22.56 lever-presses per min, respectively, for the four groups as listed in Table 1. Mean suppression ratios during testing are shown in Fig. 2. As Fig. 2 shows, we observed a strong deflation effect, regardless of the number of Phase 2 trials, but no inflation effects. A two-way ANOVA (Group [between-subjects]  Test CS [X vs. Y, within-subjects]) revealed a main effect of Test CS, F ð1; 44Þ ¼ 8:11; p < :01. Suppression to X was higher than suppression to Y following 16 deflation trials (X vs. Y, Group Low Def), F ð1; 44Þ ¼ 5:66; p < :05, and 64 deflation trials (X vs. Y, Group Hi Def), F ð1; 44Þ ¼ 5:39; p < :05. Conversely, suppression to X did not differ from suppression to Y following 16 inflation trials (X vs. Y, Group Low Inf), p > :90 or 64 inflation trials (X vs. Y, Group Hi Def), p > :30. Clearly, there was no effect on suppression to X of the number of Phase 2 trials, either with the deflation (X, Low Def vs. Hi Def), p > :40, or inflation (X, Low Inf vs. Hi Inf), p > :40, manipulation. One might entertain the possibility that the observed difference between the deflation and inflation conditions in this experiment stemmed, not from resistance to decreases in stimulus control (due to posttraining associative inflation of comparator stimuli) being greater than resistance to increases in stimulus control (due to defla-

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Fig. 2. Mean suppression ratios in Experiment 1. Gray bars show responding to CS X; striped bars depict responding to CS Y. Posttraining associative revaluation treatment is indicated on the horizontal axis; Def ¼ deflation; Inf ¼ inflation. A mean of zero represents maximal conditioned suppression; 0.5 represents no suppression. Error bars represent standard error of the means.

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tion of comparator stimuli), but from the inflation groups alone receiving USs in Phase 2. This could have produced enhanced fear of the context that in turn might have generally increased suppression, thereby masking a decrease in suppression to X as a result of associative inflation of A. However, this account is implausible because, if an excitatory context somehow increased suppression to X, a comparable increase would be expected to Y, which was conditioned and tested in the same context as X. Thus, any augmented suppression to X due to enhanced fear of the context should have been seen in responding to Y as well. This would have permitted any effect of inflation of A per se to still be seen as a difference in responding between X and Y. The observed similarity in suppression to X and Y argues against context conditioning masking an effect of posttraining inflation of A on X. The data from Experiment 1 replicate the previously observed asymmetry between posttraining inflation and deflation in situations where the target CS is biologically significant at the time of revaluation treatment (Phase 2 in this experiment). Whereas responding to the target CS could be readily increased through deflation of its companion stimulus, responding to the target CS could not be attenuated through inflation of a companion stimulus, even when comparable moderate baseline response levels were established for the control CS Y. Thus, these data suggest that prior failures to observe posttraining inflation effects were not the result of a ceiling created by strong responding in baseline controls. The greater difficulty in obtaining inflation than deflation effects is consistent with the comparator hypothesis assumption that inflation of the comparator stimulus–US association (Link 3) also deflates the target CS–comparator association (Link 2). Alternately, the asymmetry may simply be the result of differences in biological significance; perhaps it is more difficult to decrease an existing potential for conditioned responding than to

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establish such a potential, which might be viewed as a ÔconservativeÕ strategy favored by ecological pressures. Experiment 2

Method

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Experiment 2 was analogous to Experiment 1 with the exception that the target CSs were prevented from acquiring biological significance until after the completion of revaluation treatment. The goal was to compare the magnitude of inflation and deflation effects in a situation that minimized biological significance at the time of the revaluation treatment (Phase 2). This was achieved by using a sensory preconditioning procedure (Brogden, 1939), in which a relatively neutral stimulus acted as a ÔsurrogateÕ (S) outcome which was made biologically significant through pairings with a footshock US following the revaluation treatment. In Phase 1, all subjects received overshadowing treatment; two compound CSs were paired with the surrogate US, S (AX–S/BY–S; see Table 2). In Phase 2, overshadowing stimulus A was either associatively deflated (i.e., presented alone) or inflated (i.e., given further pairings with S), and the number of trials was manipulated. In Phase 3, the surrogate outcome, S, was paired with the footshock US. As in Experiment 1, responding to CS Y should not have been affected by posttraining associative manipulation of A and therefore it served as a within-group control for stimulus specificity of any effect of the revaluation treatments.

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Subjects and apparatus Subjects were 24 male and 24 female, experimentally naive, Sprague–Dawley descended rats obtained from our breeding colony. Body-weight ranges were 240–350 g for males and 160–230 g for females. Subjects were randomly assigned to one of four groups (ns ¼ 12), counterbalanced within groups for sex. The animals were housed and maintained as in Experiment 1. The apparatus was also identical to Experiment 1.

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Table 2 Design summary of Experiment 2 Group

Phase 1

Phase 2

Phase 3

Test

Low deflation High deflation Low inflation High inflation

AX–S/BY–S AX–S/BY–S AX–S/BY–S AX–S/BY–S

16 64 16 64

S–US S–US S–US S–US

X? X? X? X?

A– A– A–S A–S

Y? Y? Y? Y?

Note. Group names denote the amount (High vs. Low) of Phase 2 posttraining revaluation (inflation or deflation) treatment of the overshadowing stimulus (A). CSs A and B were a white noise and a buzzing stimulus, counterbalanced within groups and more salient than target CSs X and Y; CSs X and Y were a click train and a tone, counterbalanced within groups. ÔSÕ was a flashing light stimulus that served as an outcome (a surrogate US). The US was a mild footshock. Trials on either side of Ô/Õ were interspersed within each session. Ô–Õ denotes nonreinforcement.

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Procedure Acclimation and bar-press shaping (Days 1–5) were the same as in Experiment 1. Phase 1 (Overshadowing training). On Days 6 and 7, all groups received 60-min sessions of overshadowing training with two compound CSs paired with a surrogate US S (AX–S/BY–S). All CSs were 60 s in duration, and the surrogate US, S, was 5 s in duration. The onset of the surrogate US coincided with the termination of the CSs. Two such trials with each compound CS per day were interspersed among intertrial intervals of 12  4 min (as measured from trial termination to trial onset), and trial orders were counterbalanced within groups. As in Experiment 1, the tone and click served as target CSs X and Y, counterbalanced within groups, and the more salient white noise and buzzer served as the overshadowing CSs A and B, counterbalanced within groups. The flashing light served as the surrogate US for all subjects. Phase 2 (Revaluation). On Days 8–11, subjects received either inflation (Inf) or deflation (Def) of the overshadowing stimulus A. Deflation groups received 16 (Low Def) or 64 (Hi Def) presentations of A-alone, whereas inflation groups received 16 (Low Inf) or 64 (Hi Inf) pairings of A with the surrogate US, S (A–S). The onset of the 5-s surrogate US coincided with the termination of the 60-s CSs. Intertrial intervals were 5  2 min. Session durations were 80 min for the Hi groups and 20 min for the Low groups. Phase 3 (Training with S). On Days 12 and 13, for all subjects, the surrogate US, S, was paired with a 0.5-s, 0.55-mA footshock US (S–US). Notably, the intensity of footshock was higher in Experiment 2 than Experiment 1 because we wanted to obtain similar baseline conditioned suppression between the two experiments and we knew, all other things being equal, that the sensory precondition of Experiment 2 would support less suppression than the first-order conditioning of Experiment 1. The onset of the footshock coincided with the termination of the 5-s S presentations. Four such trials were scheduled per day and separated by intertrial intervals of 12  4 min within each 60-min session. Restabilization of bar pressing and testing was the same as in Experiment 1. Results and discussion

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A one-way ANOVA of baseline lever-press rates during the last session of restabilization revealed no main effect of Group, p > :40. Baseline response rates at this time (one day prior to the start of testing) were 19.04, 21.50, 24.37, and 22.26 lever-presses per min, respectively, for the four groups as listed in Table 2. Mean suppression ratios during testing are plotted in Fig. 3. As shown in Fig. 3, we observed both strong inflation and strong deflation effects regardless of the number of Phase 2 trials. A two-way ANOVA (Group [betweensubjects]  Test CS [X vs. Y, within-subjects]) revealed a main effect of Group, F ð3; 44Þ ¼ 7:41; p < :01, and an interaction, F ð3; 44Þ ¼ 9:19; p < :01. Suppression to X was higher than suppression to Y following 16 deflation trials (X vs. Y, Group Low Def), F ð1; 44Þ ¼ 4:14; p < :05, as well as 64 deflation trials (X vs. Y, Group Hi Def), F ð1; 44Þ ¼ 4:30; p < :05. Conversely, suppression to X was lower than Y following 16 inflation trials (X vs. Y, Group Low Inf), F ð1; 44Þ ¼ 9:89; p < :01, as well

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Fig. 3. Mean suppression ratios in Experiment 2. Gray bars show responding to CS X; striped bars depict responding to CS Y. Posttraining associative revaluation treatment is indicated on the horizontal axis; Def ¼ deflation; Inf ¼ inflation. A mean of zero represents maximal conditioned suppression; 0.5 represents no suppression. Error bars represent standard error of the means.

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as 64 inflation trials (X vs. Y, Group Hi Inf), F ð1; 44Þ ¼ 12:21; p < :01. There was no effect on suppression to X of the number of Phase 2 trials for either deflation (X, Low Def vs. Hi Def), p > :40, or inflation (X, Low Inf vs. Hi Inf), p > :40. In sum, the present data suggest that the magnitude of inflation and deflation effects is symmetrical in a situation that minimizes the biological significance of the target CSs (e.g., sensory preconditioning). Importantly, the symmetry between inflation and deflation in sensory preconditioning (i.e., with stimuli of low biological significance) argues against the comparator hypothesis account of the asymmetry with stimuli of high biological significance. The comparator hypothesis anticipates that deflation effects should occur more readily regardless of biological significance. Presumably, in the comparator framework, the inflation manipulation strengthens the comparator stimulus–US association (Link 3 of Fig. 1) but at the same time weakens the association between the target CS and its comparator stimulus (Link 2). The symmetry between inflation and deflation observed when biological significance is minimized suggests that decrements in Link 2 do not play a major role in minimizing deflation effects in first-order conditioning. Instead, biological significance appears to afford a stimulus some degree of protection against reductions in its control over responding. That is, once a stimulus elicits a vigorous response (i.e., acquires biological significance), subsequent reductions of responding through posttraining inflation are difficult to obtain. However, if the stimulus does not yet control behavior (i.e., it is of low biological significance), then posttraining inflation effects can be obtained as readily as deflation effects. Thus, the protection afforded biologically significant cues against cue competition is a constraint which appears to delimit the domain of the comparator hypothesis.

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An obvious question raised by the first two experiments is whether a stimulusÕ being biologically significant protects it specifically against reductions in overt responding as a result of associative inflation of its comparator stimulus, or whether it also protects it against reductions in its potential to serve as a comparator stimulus for another stimulus. One way to answer this question is by establishing a biologically significant CS that is also a comparator stimulus for a second CS. The prior experiments suggested that the first CS will be protected against decreases in responding to it as a consequence of posttraining inflation of its comparator stimulus. The question here is whether such posttraining inflation will nevertheless decrease the comparator value of the first CS in modulating responding to the second CS; that is, will an increase in responding to the second CS be observed? This question might be viewed through the framework of the Ôextended comparator hypothesis,Õ which was proposed recently by Denniston, Savastano, and Miller (2001; see also Stout, Savastano, & Miller, 2003). The extended comparator hypothesis posits that the effectiveness of a comparator stimulus is itself modulated by a (second-order) comparator stimulus. Specifically, it predicts that second-order comparator stimuli inversely modulate the effectiveness of first-order comparator stimuli, and consequently should have a direct effect on responding to the target CS. Thus, associative inflation of a second-order comparator stimulus should increase responding to the target CS, whereas deflation should decrease responding. Exactly these symmetrical (opposing) results have been obtained in situations in which the target CS is not biologically significant prior to the comparator revaluation treatment (i.e., embedded within Phase 1 of sensory preconditioning; e.g., Stout et al., 2003). In the framework of the extended comparator hypothesis, these results are a consequence of the second-order comparator stimulus modulating the effectiveness of a first-order comparator stimulus. In the present experiment, we compared the effects of inflating and deflating the associative status of so-called second-order comparator stimuli in a situation in which the target CS (and its first-order comparator stimulus) was biologically significant. Just as deflation (but not inflation) of a first-order comparator stimulus can influence responding to a biologically significant target CS, so deflation of a second-order comparator stimulus might be expected to influence (enhance) the associative status (and consequently the comparator value) of the first-order comparator stimulus. But, if biologically significant stimuli are partially protected from revaluation effects that would otherwise decrease (down modulate) their control of behavior, this enhancement of the associative status of the first-order comparator stimulus should not reduce responding to the target CS. Moreover, posttraining inflation of a second-order comparator stimulus should not down modulate the comparator value of a biologically significant first-order comparator stimulus, just as posttraining inflation of a first-order comparator stimulus does not down modulate responding to a target CS. That is, if posttraining inflation and deflation of a target CSÕs secondorder comparator stimulus influence responding to the target CS by modulating the comparator value of a first-order comparator stimulus, the effectiveness of biologically significant first-order comparator stimuli should not be affected by inflation

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of the second-order comparator stimulus. Thus, if the first-order comparator stimulus is biologically significant, inflation of second-order comparator stimuli should not result in increased responding to the target CS. Alternatively, associative status as it influences response potential and associative status as indexed by comparator potential might be different variables. That is, the biological significance of a first-order comparator stimulus might protect it against a loss in response potential when its own (second-order) comparator stimulus is inflated, but allow it to lose comparator value, thereby allowing posttraining inflation of the second-order comparator stimulus to increase in responding to the target CS. If posttraining inflation of a second-order comparator stimulus enhances responding to a target CS, it would suggest that biological significance affords a (first-order comparator) stimulus protection only from decreases in response potential and not from decreases in comparator value. In Phase 1, all subjects received overshadowing treatment with two compound CSs, with CS X as a common element (AX–US/XY–US; see Table 3). In this treatment, the overshadowing stimulus A should serve as the (first-order) comparator stimulus for target CS X, and X presumably would serve as the first-order comparator stimulus for target CS Y. In turn, the overshadowing stimulus (A) should serve as a second-order comparator for target CS Y. In Phase 2, either the overshadowing stimulus A or an irrelevant stimulus (B) was either associatively deflated or inflated. According to the extended comparator hypothesis, if the biological significance of the stimuli had no effect, associative deflation of A would be expected to increase responding to X (for which A was a first-order comparator) and also decrease responding to Y (for which A was a second-order comparator). Conversely, associative inflation of A should decrease responding to X and increase responding to Y. However, because Experiment 3 was not conducted in sensory preconditioning, biological significance was expected to prevent the first-order inflation effect. The question here is whether second-order comparator effects would show a similar asymmetry.

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Table 3 Design summary of Experiment 3 Group

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Phase 2

Phase 3

Test

Deflation control Inflation control Deflation Inflation

AX–US/XY–US AX–US/XY–US AX–US/XY–US AX–US/XY–US

B– B–US A– A–US

S– S– S– S–

X? X? X? X?

Y? Y? Y? Y?

Note. Group names denote the Phase 2 posttraining revaluation (inflation or deflation) treatment of the overshadowing stimulus (A) or an irrelevant stimulus (B). CSs A and B were a white noise and a buzzing stimulus, counterbalanced and more salient than target CSs X and Y; CSs X and Y were a click train and a tone, counterbalanced within groups. The US was a mild footshock. ÔSÕ was a flashing light stimulus that served as an outcome (a surrogate US) in Experiment 2; it had no direct relevance to Experiment 1 and was included only to increase the equivalence between experiments. Trials on either side of Ô/Õ were interspersed within each session. Ô–Õ denotes nonreinforcement.

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Subjects and apparatus Subjects were 48 male and 48 female, experimentally naive, Sprague–Dawley descended rats obtained from our breeding colony. Body-weight ranges were 260–355 g for males and 170–300 g for females. Subjects were randomly assigned to one of four groups (ns ¼ 24), counterbalanced within groups for sex. The animals were housed and maintained as in the previous experiments. The apparatus was also identical to the previous experiments.

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Procedure Acclimation and bar-press shaping (Days 1–5) were the same as in the previous experiments. Phase 1 (Overshadowing training). On Days 6 and 7, all groups received daily 60min sessions of training with two compound CSs (AX and XY). The compound CSs were paired with a 0.5-s, 0.50-mA footshock US (AX–US/BY–US). All CSs were 60 s in duration. The onset of the US coincided with the termination of the CSs. There were two trials per day with each compound CS, interspersed, with intertrial intervals of 12  4 min (measured from trial termination to trial onset), and trial orders were counterbalanced within groups. The tone and click served as target CSs X and Y, counterbalanced within groups. The more salient white noise and buzzer served as the overshadowing CSs A and B, counterbalanced within groups. Phase 2 (Revaluation). On Days 8–12, subjects received either inflation (Inf) or deflation (Def) of the overshadowing stimulus (A) or another (associatively irrelevant) stimulus (B). Deflation groups received 80 presentations (16/day) of either A (Deflation) or B (Deflation Control) alone. Inflation groups received 80 pairings (16/day) of A (Inflation) or B (Inflation Control) with the US. The onset of the US coincided with the termination of the 60-s CSs. Intertrial intervals were 5  2 min. The daily sessions were 80 min in duration. Phase 3 (Dummy exposure to S). On Days 13 and 14, all subjects were exposed to Stimulus S (the flashing-light surrogate US used in Experiment 2) alone, just as in Phase 3 of Experiment 1. Four presentations per day were scheduled and separated by intertrial intervals of 12  4 min within the 60-min session. In this experiment, Stimulus S played no relevant role. Phase 3 was included to only to equate retention intervals, handling, and exposure to Stimulus S with Experiment 2. Restabilization of bar pressing and testing was the same as in the previous experiments. Results and discussion Due to experimenter error in Phase 2, data from four subjects per group were lost. Thus, for the following analysis, the actual n per group is 20. A one-way ANOVA of baseline lever-press rates during the last session of restabilization revealed no main effect of Group, p > :45. Baseline response rates at this time (one day prior to the start of testing) were 20.41, 23.80, 25.32, and 21.55 lever-presses per min,

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respectively, for the four groups listed in Table 3. Mean suppression ratios during testing are plotted in Fig. 4. As expected, there was an asymmetrical effect of inflation and deflation of the overshadowing stimulus A on responding to target CS X, but there was no effect of inflation or deflation of A on responding to target CS Y. A three-way ANOVA (Revaluation treatment [Deflation vs. Inflation, between-subjects]  Group [Control vs. Experimental, between-subjects]  Test CS [X vs. Y, within-subjects]) revealed main effects of Revaluation treatment, F ð1; 72Þ ¼ 4:19; p < :05, and Test CS, F ð1; 72Þ ¼ 5:88; p < :05. Groups that received a larger total number of shocks (Groups Inflation and Inflation Control) showed greater overall suppression than the deflation groups. Presumably, this was a nonassociative effect. Consequently, no further comparisons were made between the inflation and deflation groups. Suppression to X was higher in Group Deflation than Group Deflation Control, F ð1; 72Þ ¼ 5:32; p < :05, showing an effect of extinguishing (deflating) XÕs first-order comparator stimulus (A). However, suppression to Y in those groups was unaffected by this deflation manipulation, p > :80, indicating that there was no effect of extinguishing the second-order comparator for Y (also A). As expected, there was no effect of posttraining inflation of A (Groups Inflation vs. Inflation Control) on responding to X, p > :40. Less expectedly, inflation of A had no effect on responding to Y for which A was a second-order comparator stimulus, p > :40. One might ask if context conditioning in the inflation condition might have masked an effect of posttraining inflation of A on responding to X in the present experiment. However, the same argument discounting context conditioning as a factor

Fig. 4. Mean suppression ratios in Experiment 3. Gray bars show responding to CS X; striped bars depict responding to CS Y. Posttraining associative revaluation treatment is indicated on the horizontal axis; Def ¼ deflation; Inf ¼ inflation. A mean of zero represents maximal conditioned suppression; 0.5 represents no suppression. Error bars represent standard error of the means.

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in not seeing an effect of inflation of A in Experiment 1 (see the third paragraph of the Result section of Experiment 1) applies to any possible role of context conditioning in the inflation condition of this experiment. In sum, Experiment 3 replicated previous failures to observe an effect of inflation of a first-order comparator stimulus and successes in obtaining a first-order comparator deflation effect, when the target stimulus has acquired biological significance. More interesting is the result that neither inflation nor deflation of the overshadowing stimulus (YÕs second-order comparator stimulus) altered conditioned responding to Y. Thus, neither second-order inflation nor deflation effects are readily obtained in situations in which the target stimulus has high biological significance at the time of retrospective revaluation treatment. This result contrasts markedly with those of several recent studies in our laboratory that used a similar preparation and parameters, which demonstrated an effect of posttraining manipulation of second-order comparator stimuli on target stimuli with low biological significance (i.e., in sensory preconditioning procedures; Blaisdell, Bristol, Gunther, & Miller, 1998; Denniston, Savastano, Blaisdell, & Miller, 2003; Denniston, Savastano, & Miller, 2001; Stout et al., 2003). For purposes of comparison to the results of Experiment 3, we here summarize Experiment 2 of Stout et al. (2003) because it so closely paralleled Experiment 3 in subjects (rats), task (suppression of conditioned lever press for water), parameters, and procedures, except that target training and retrospective revaluation treatment were embedded in a sensory preconditioning procedure so that the target stimulus was not biologically significant at the time after target training that its second-order comparator stimulus was associatively inflated or deflated (see Table 4). (This study is not fully reported here because it was performed to make another point essential to the focus of Stout et al. (2003).) In Phase 1 of this study, highly salient cue A was compounded with less salient cue X and paired with [neutral] outcome S (i.e., AX–S). These trials were interspersed with pairings of compound XY (X and Y being of equal salience and counterbalanced) with outcome S (i.e., XY–S). In Phase 2, A or X was associatively inflated (i.e., A–S or X–S) or deflated (i.e., A– or X–); a Table 4 Design and result summary of Stout et al. (2003, Experiment 2)

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Inflate X Inflate A Deflate Deflate A None

Phase 1

AX–S/XY–S AX–S/XY–S AX–S/XY–S AX–S/XY–S AX–S/XY–S

Phase 2

X–S A–S X– A– Cntxt only

Phase 3

S–US S–US S–US S–US S–US

Test X?

Y?

0.17 0.34 0.34 0.20 0.25

0.28 0.19 0.20 0.34 0.13

Note. Group names denote Phase 2 treatment (posttraining revaluation of A or X or no revaluation). CS A was more salient than CSs X and Y, which were of equal salience and physically counterbalanced within groups. ÔSÕ was an initially neutral stimulus that served as an outcome (a surrogate US). The US was a mild footshock. Trials on either side of Ô/Õ were interspersed within each session. Ô–Õ denotes nonreinforcement. Test results are lever-press suppression scores with 0.50 indicating no suppression and 0 indicating total suppression during test trial presentations of the CS (X and Y).

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control group (None) received only brief exposure to the experimental context during Phase 2. In Phase 3, S was paired with a mild footshock (i.e., S–US). Finally, subjects were tested on Y and X in counterbalanced order. Table 4 lists the suppression rates for X and Y for each group of Stout et al.Õs (2003) Experiment 2. Despite Group None receiving more X–S pairings than Y–S pairings, X was observed to have less control of behavior presumably because of its strong association with A, which itself was strongly associated with S due to AÕs high salience. That is, the X–A and A–S associations presumably down modulated the effectiveness of the X–S association, relative to the Y–S association. Given that A presumably down modulated the effectiveness of X both as an elicitor of behavior and as a first-order comparator stimulus for Y, suppression to Y by Group None was strong, and possibly approached the greatest suppression possible given the weak footshock with which S was paired. Posttraining inflation of X (Group Inflate X) not only increased suppression to X but decreased suppression to Y relative to control Group None. (Deflation of X decreased suppression to X but likely due to a floor effect imposed by the weak footshock did not further increase suppression to Y.) More important to the present issue, in Group Deflate A deflation of A (XÕs first-order comparator stimulus and YÕs secondorder comparator stimulus) tended to increase suppression to X and greatly decreased suppression to Y relative to Group None. (Inflation of A decreased suppression to X but, due to the floor effect imposed by the weak footshock, did not further increase suppression to Y.) For present purposes, the critical observation here is that in posttraining manipulations of A not only influenced responding to X (e.g., Group Inflate A) but also influenced responding to Y (e.g., Group Deflate A). This is in stark contrast to the present Experiment 3 in which posttraining manipulations of A failed to influence stimulus control by Y. The only significant difference between these two studies is that the present Experiment 3 was done with first-order conditioning, whereas the Stout et al. (2003) study was embedded in a sensory preconditioning procedure. Thus, we see that when a comparator stimulus (X) is not of high biological significance at the time of retrospective revaluation treatment (due to the use of sensory preconditioning in this case), posttraining deflation of the comparator stimulusÕ (X) own comparator stimulus (A; i.e., the targetÕs second-order comparator stimulus) attenuates subsequent stimulus control by the target. In summary, biologically significant stimuli not being susceptible to either inflation or deflation of the associative status of a second-order comparator stimulus implies that high biological significance not only provides protection to a stimulus from reductions in responding due to posttraining inflation of its [first-order] comparator stimulus. At least with the present parameters, high biological significance also provides protection to a [first-order comparator] stimulus from reductions in its comparator value due to inflation of itÕs own comparator stimulus.

General discussion Posttraining decreases in the associative strength (i.e., associative deflation) of a companion stimulus can increase responding to a target stimulus, a phenomenon that has now been replicated across various tasks and species. However, the converse

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effect has proven more difficult to achieve: Posttraining increases (i.e., associative inflation) of a companion stimulus often fail to decrease responding to the target stimulus. Notably, inflation effects have occurred only in situations where the target stimulus was prevented from acquiring biological significance until after completion of all other training manipulations, for example, backward blocking embedded in sensory preconditioning or in human tasks with outcomes of low inherent biological significance (but see Larkin et al., 1998). However, it was unclear whether failures to observe posttraining inflation effects with biologically significant stimuli were due to extremely high levels of responding (i.e., a ceiling effect), rather than a principled difficulty in obtaining these effects. The present studies compared the magnitude of inflation and deflation effects against a common baseline that minimized ceiling and floor effects. Experiment 1 replicated the asymmetry between inflation and deflation with stimuli of high biological significance. In contrast, Experiment 2 demonstrated symmetrical inflation and deflation effects when biological significance was minimized by embedding the critical phases of treatment within a sensory preconditioning procedure. This observation must to some degree be qualified because a few experimenters using human subjects with outcomes of low biological significance have found asymmetrical results; however, when they have, the asymmetry has not been consistently toward more deflation than inflation [compare Larkin et al., 1998 with Van Hamme and Wasserman (1994)]. Based upon these findings, biologically significant stimuli appear to be relatively immune to reductions in stimulus control of behavior. That is, once a stimulus elicits a vigorous response, decreases in responding to that stimulus as a consequence of posttraining inflation of its companion stimulus are difficult to obtain (e.g., Blaisdell, Denniston, Savastano, & Miller, 2000; Oberling, Bristol, Matute, & Miller, 2000). However, if the stimulus does not yet control behavior (i.e., if it is of low biological significance), then posttraining inflation effects can be obtained. In contrast, increases in responding to a stimulus as a result of posttraining deflation of its companion stimulus are readily observed, provided ceiling effects are avoided and sufficient deflation treatment is administered. This asymmetry in the relative facility of increasing versus decreasing conditioned responding does not appear to be a function solely of baseline levels of responding. More generally, the effect of biological significance on the relative effectiveness of inflation and deflation parallels the differences in the rates of simple Pavlovian acquisition and extinction. It is well known that the acquisition of a conditioned response typically proceeds much faster than its extinction (Pavlov, 1927). Our finding that inflation and deflation effects are symmetrical when the stimuli are of low biological significance challenges the comparator hypothesis account of the asymmetry observed with biologically significant stimuli. Specifically, if the greater difficulty in obtaining inflation than deflation effects were solely due to the fact that inflation weakens the target CS–comparator association (Link 2), then an asymmetry should have occurred in Experiment 2. Thus, the symmetry observed in Experiment 2 appears to establish low biological significance of the target stimulus as a boundary condition for the inflation effects predicted by the comparator hypothesis. However, other models, including recently proposed learning-focused models of

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acquired behavior that were designed to account for the effects of posttraining inflation and deflation (e.g., Tassoni, 1995; Van Hamme & Wasserman, 1994), as well as recently proposed performance-focused models (e.g., Gallistel & Gibbon, 2000), are equally challenged. Most of these models predict symmetrical effects of posttraining inflation and deflation, and fail to predict the interaction with biological significance. However, the learning-focused model of Dickinson and Burke (1996), with appropriate parameters, predicts stronger deflation effects and inflation effects (Larkin et al., 1998), but fails to predict why this asymmetry is attenuated when the target CS is not biologically significant. Experiment 3 (in conjunction with Stout et al., 2003, Experiment 2) addressed the question of whether biological significance protects specifically against reductions in conditioned responding or whether it also protects the comparator value of a stimulus against reduction. According to the extended comparator hypothesis (Denniston et al., 2001; see also Stout et al., 2003), the effectiveness of a comparator stimulus is itself modulated by a (second-order) comparator stimulus. Specifically, second-order comparator stimuli are presumed to alter the effectiveness of first-order comparator stimuli, and thus should have a direct effect on responding to the target CS. Consequently, associative inflation of a second-order comparator stimulus should increase responding to the target CS, whereas deflation should decrease responding. These second-order comparator inflation and deflation effects have been confirmed recently with stimuli of low biological significance (i.e., in sensory preconditioning procedures; Blaisdell et al., 1998; Denniston et al., 2003; Denniston et al., 2001; Stout et al., 2003). However, Experiment 3 showed neither second-order inflation nor deflation effects are obtained with stimuli of high biological significance, whereas manipulations of second-order comparator stimuli were seen to occur when the same procedure was embedded in a sensory-preconditioning procedure (Stout et al., 2003, Experiment 2). These results suggest that biological significance provides protection against a stimulus losing either response potential or comparator value as a result of posttraining inflation of its comparator stimulus.

References

R

Arcediano, F., Escobar, M., & Matute, M. (2001). Reversal from blocking in humans as a result of posttraining extinction of the blocking stimulus. Animal Learning & Behavior, 29, 354–366. Best, M. R., Dunn, D. P., Batson, J. D., Meachum, C. L., & Nash, S. M. (1985). Extinguishing conditioned inhibition in flavour-aversion learning: Effects of repeated testing and extinction of the excitatory element. Quarterly Journal of Experimental Psychology B, 37, 359–378. Blaisdell, A. P., Bristol, A. S., Gunther, L. M., & Miller, R. R. (1998). Overshadowing and latent inhibition counteract each other: Support for the comparator hypothesis. Journal of Experimental Psychology: Animal Behavior Processes, 24, 335–351. Blaisdell, A. P., Denniston, J. C., & Miller, R. R. (2001). Recovery from the overexpectation effect: Contrasting performance-focused and acquisition-focused models of retrospective revaluation. Animal Learning & Behavior, 29, 367–380. Blaisdell, A. P., Denniston, J. C., Savastano, H. I., & Miller, R. R. (2000). Counterconditioning of an overshadowed cue attenuates overshadowing. Journal of Experimental Psychology: Animal Behavior Processes, 26, 74–86.

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323

R

ET

R

AC

TE

D

Blaisdell, A. P., Gunther, L. M., & Miller, R. R. (1999). Recovery from blocking through deflation of the block stimulus. Animal Learning & Behavior, 27, 63–76. Brogden, W. J. (1939). Sensory preconditioning. Journal of Experimental Psychology, 25, 323–332. Chapman, G. B. (1991). Trial order affects cue interaction in contingency judgment. Journal of Experimental Psychology: Learning, Memory, and Cognition, 17, 837–854. Cole, R. P., Barnet, R. C., & Miller, R. R. (1995). Effect of relative stimulus validity: Learning or performance deficit? Journal of Experimental Psychology: Animal Behavior Processes, 21, 293–303. Denniston, J. C., Savastano, H. I., Blaisdell, A. P., & Miller, R. R. (2003). Cue competition as a performance deficit. Learning and Motivation, 34, 1–31. Denniston, J. C., Miller, R. R., & Matute, H. (1996). Biological relevance as a determinant of cue competition. Psychological Science, 7, 325–331. Denniston, J. C., Savastano, H. I., & Miller, R. R. (2001). The extended comparator hypothesis: Learning by contiguity, responding by relative strength. In R. R. Mowrer, & S. B. Klein (Eds.), Handbook of contemporary learning theories (pp. 65–117). Hillsdale, NJ: Erlbaum. Dickinson, A., & Burke, J. (1996). Within-compound associations mediate the retrospective revaluation of causality judgments. Quarterly Journal of Experimental Psychology B, 49, 60–80. Dickinson, A., & Charnock, D. J. (1985). Contingency effects with maintained instrumental reinforcement. Quarterly Journal of Experimental Psychology B, 37, 397–416. Feldman, J. M. (1975). Blocking as a function of added cue intensity. Animal Learning & Behavior, 3, 98–102. Gallistel, C. R., & Gibbon, J. (2000). Time, rate, and conditioning. Psychological Review, 107, 289–344. Grahame, N. J., Barnet, R. C., & Miller, R. R. (1992). Pavlovian inhibition cannot be obtained by posttraining A–US pairings: Further evidence for the empirical asymmetry of the comparator hypothesis. Bulletin of the Psychonomic Society, 30, 399–402. Holland, P. C. (1999). Overshadowing and blocking as acquisition deficits: No recovery after extinction of overshadowing or blocking cues. Quarterly Journal of Experimental Psychology B, 52, 307–334. Kasprow, W. J., Schachtman, T. R., & Miller, R. R. (1987). The comparator hypothesis of conditioned response generation: Manifest conditioned excitation and inhibition as a function of relative excitatory strengths of CS and conditioning context at the time of testing. Journal of Experimental Psychology: Animal Behavior Processes, 13, 395–406. Kaufman, M. A., & Bolles, R. C. (1981). A nonassociative aspect of overshadowing. Bulletin of the Psychonomic Society, 18, 318–320. Koksal, F., Domjan, M., & Weisman, G. (1994). Blocking of the sexual conditioning of differentially effective conditioned stimulus objects. Animal Learning & Behavior, 22, 103–111. Larkin, M. J. W., Aitken, M. R. F., & Dickinson, A. (1998). Retrospective revaluation of causal judgments under positive and negative contingencies. Journal of Experimental Psychology: Learning, Memory, and Cognition, 24, 1331–1352. LoLordo, V. M., Jacobs, W. J., & Foree, D. D. (1982). Failure to block control by a relevant stimulus. Animal Learning & Behavior, 10, 183–193. Lysle, D. T., & Fowler, H. (1985). Inhibition as a ‘‘slave’’ process: Deactivation of conditioned inhibition through extinction of conditioned excitation. Journal of Experimental Psychology: Animal Behavior Processes, 11, 71–94. Matzel, L. D., Schachtman, T. R., & Miller, R. R. (1985). Recovery of an overshadowed association achieved by extinction of the overshadowing stimulus. Learning and Motivation, 16, 398–412. Miller, R. R., Hallam, S. C., & Grahame, N. J. (1990). Inflation of comparator stimuli following CS training. Animal Learning & Behavior, 18, 434–443. Miller, R. R., Hallam, S. C., Hong, J. Y., & Dufore, D. S. (1991). Associative structure of differential inhibition: Implications for models of conditioned inhibition. Journal of Experimental Psychology: Animal Behavior Processes, 17, 141–150. Miller, R. R., & Matute, H. (1996). Biological significance in forward and backward blocking: Resolution of a discrepancy between animal conditioning and human causal judgment. Journal of Experimental Psychology: General, 125, 370–386.

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Miller, R. R., & Matzel, L. D. (1988). The comparator hypothesis: A response rule for the expression of associations. In G. H. Bower (Ed.), The psychology of learning and motivation: Vol. 22 (pp. 51–92). San Diego, CA: Academic Press. Miller, R. R., & Schachtman, T. R. (1985). Conditioning context as an associative baseline: Implications for response generation and the nature of conditioned inhibition. In R. R. Miller, & N. E. Spear (Eds.), Information processing in animals: Conditioned inhibition (pp. 51–88). Hillsdale, NJ: Erlbaum. Oberling, P., Bristol, A., Matute, H., & Miller, R. R. (2000). Biological significance attenuates overshadowing, relative validity, and degraded contingency effects. Animal Learning & Behavior, 28, 172–186. Pavlov, I. P. (1927). Conditioned reflexes. London: Oxford University Press. Rauhut, A. S., McPhee, J. E., DiPietro, N. T., & Ayres, J. J. B. (2000). Conditioned inhibition training of the competing cue after compound conditioning does not reduce cue competition. Animal Learning & Behavior, 28, 92–108. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black, & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64–99). New York: Appleton-Century-Crofts. Schachtman, T. R., Brown, A. M., Gordon, E. L., Catterson, D. A., & Miller, R. R. (1987). Mechanisms underlying retarded emergence of conditioned responding following inhibitory training: Evidence for the comparator hypothesis. Journal of Experimental Psychology: Animal Behavior Processes, 13, 310–322. Schweitzer, L., & Green, L. (1982). Reevaluation of things past: A test of the ‘‘retrospective hypothesis’’ using a CER procedure with rats. Pavlovian Journal of Biological Science, 17, 62–68. Shanks, D. R. (1985). Forward and backward blocking in human contingency judgement. Quarterly Journal of Experimental Psychology B, 37, 1–21. Stout, S., Savastano, H. I., & Miller, R. R. (2003). The extended comparator hypothesis. Manuscript submitted for publication. Tassoni, C. J. (1995). The least mean squares network with information coding: A model of cue learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 21, 193–204. Van Hamme, L. J., & Wasserman, E. A. (1994). Cue competition in causality judgments: The role of nonpresentation of compound stimulus elements. Learning and Motivation, 25, 127–151. Wasserman, E. A., & Berglan, L. R. (1998). Backward blocking and recovery from overshadowing in human causality judgment: The role of within-compound associations. Quarterly Journal of Experimental Psychology B, 51, 121–138. Williams, D. A., Sagness, K. E., & McPhee, J. E. (1994). Configural and elemental strategies in predictive learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 20, 694–709.