Temporal integration in second-order conditioning and sensory preconditioning

Lick suppression experiments with rats revealed that the magnitude of both second-order conditioning (Experiment 1) and sensory preconditioning (Experiment 2) was superior when that conditioning was based on backward (US→CS) relative to forward (CS→US) first-order pairings of a CS and US. The superiority of backward relative to forward first-order conditioning on suppression to the higher order cues can be understood by assuming that the magnitude of higher order conditioning was determined by a memory representation of the higher order cues that provided information about the expected temporal location of the US. The results suggest that temporal information such as order between paired CSs and USs was encoded, preserved, and integrated with memory for the higher order stimuli. The relevance of these findings to memory integration in Pavlovian learning, the temporal coding hypothesis (Barnet, Arnold, & Miller, 1991; Matzel, Held, & Miller, 1988), backward excitatory conditioning, and the associative structure that underlies second-order Pavlovian fear conditioning are discussed.     

Associative structure of integrated temporal relationships

According to the temporal-coding hypothesis (TCH; Savastano & Miller, Behavioural Processes 44:147–162, 1998), acquired associations include temporal information concerning the interval between the associated elements. Moreover, the TCH posits that subjects can integrate two independently acquired associations that share a common element (e.g., S2–S1 and S1–US), which results in the creation of a third association with its own temporal relationship (S2–US). Some evidence has suggested that such temporal integration occurs at the time of testing (Molet, Miguez, Cham, & Miller, Journal of Experimental Psychology: Animal Behavior Processes 38:369–380, 2012). Here we report two fear-conditioning experiments with rats conducted to identify the associative structure of the integrated temporal relationship. The goal was to distinguish between two possible associative structures that could exist following an initial test on which temporal integration occurs: (1) Conditioned responding to S2 on subsequent tests could be the result of recurring successive activation of two independently learned temporal maps that remain independently stored in memory (i.e., S2–S1 plus S1–US). (2) Temporal integration at the moment of initial testing could result in the formation of a direct S2–US (or S2–response) temporal map. Integration was found to occur at test and to produce a new association that was independent of associations with the common element (S1). However, the associative status of S1 appeared to modulate whether or not the new association with S2 was US-specific (S2–US) or directly activated a fear response (S2–response).     

When more is less: Extending training of the blocking association following compound training attenuates the blocking effect

Three conditioned lick suppression experiments with rats were performed to assess the influence, following compound training of two stimuli (A and X) with the same outcome (AX-O trials), of extending training of the blocking association (i.e., A-O) on responding to the target stimulus (X) at test. In Experiment 1, backward blocking was attenuated when the blocking association was extensively trained. Experiment 2 showed that forward blocking was also attenuated by extensive further training of the blocking association following the AX-O trials. Experiment 3 contrasted candidate explanations of the results of Experiments 1 and 2 and demonstrated that these results are consistent with the framework of the extended comparator hypothesis (Denniston, Savastano, & Miller, 2001).     

Local context and the comparator hypothesis

“Comparator” accounts of associative conditioning (e.g., Gibbon & Balsam, 1981; Miller & Matzel, 1988) suggest that performance to a Pavlovian CS is determined, by a comparison of the US expectancy of the CS with the US expectancy of general background cues. Recent research indicates that variation in the excitatory value of cues in the local temporal context of a CS may have a profound impact on conditioned responding to the CS (e.g., Kaplan & Hearst, 1982), implicating US expectancy based on local, rather than overall, background cues as the critical comparator term for a CS. In two experiments, an excitatory training context attenuated responding to a target CS. In Experiment 1, the context was made excitatory by interspersing unsignaled USs with target CS-US trials. In this case, posttraining extinction of the conditioning context restored responding to the target CS. In Experiment 2, the target CS’s local context was made excitatory by the placement of excitatory “cover” stimuli in the immediate temporal proximity of each target CS-US trial. In this experiment, posttraining extinction of the proximal cover stimuli, not extinction of the conditioning context alone, restored responding to the target CS. An observation from both experiments was that signaling the otherwise unsignaled USs did not appear to influence the associative value of the conditioning context. The results are discussed in relation to a local context version of the comparator hypothesis and serve to emphasize the importance of local context cues in the modulation of acquired behavior. Taken together with other recent reports (e.g., Cooper, Aronson, Balsam, & Gibbon, 1990; Schachtman & Reilly, 1987), the present observations encourage contemporary comparator theories to reevaluate which aspects of the conditioning situation comprise the CS’s comparator term.     

Temporal coding in conditioned inhibition: Retardation tests

Two lick suppression experiments with rats were conducted in order to determine the nature of the temporal information that is encoded as a result of Pavlovian conditioned inhibition training (conditioned stimulus {CS} A→unconditioned stimulus {US}/AX→noUS). After inhibition training, the conditioned inhibitor (X) was paired with the US in order to measure inhibition, as assessed through retarded behavioral control by CS X. Three temporal relationships were manipulated: the A-US interval, the X-A interval of inhibition training, and the X-US interval of the retardation test pairings. Retardation was greatest when the X-US temporal relationship matched the time at which the US was expected (but not delivered) on the X-A inhibition training trials. Thus, the present experiments provide evidence with retardation tests that, during conditioned inhibition training, subjects encode the temporal location of the omitted US relative to the inhibitory CS. These findings complement those of previous studies using summation tests of conditioned inhibition (Barnet & Miller, 1996; Denniston, Blaisdell, á Miller, 1998; Denniston, Cole, & Miller, 1998).     

Discrimination blocking: Acquisition versus performance deficits in human contingency learning

We compared acquisition and performance accounts of human contingency learning. After solving a discrimination in Phase 1, in which Cue A predicted the occurrence of the outcome and Cue B predicted its nonoccurrence (A+/B−), a new discrimination (X+/Y−) was superimposed in Phase 2 (AX+/BY−). The participants were finally trained in Phase 3 with the added discrimination, which either maintained the same contingencies as those in Phase 2 (X+/Y−; Experiment 1) or reversed the contingencies (X−/Y+; Experiment 2). According to competitive-learning theories (e.g., Rescorla & Wagner, 1972), there should be no learning of the added discrimination in Phase 2, so that no advantage or disadvantage for this discrimination should be observed in Phase 3. In contrast, performance theories, such as the comparator hypothesis (Miller & Matzel, 1988), contend that learning of the added discrimination in Phase 2 should proceed normally; so, in Phase 3, an advantage for the added discrimination should be observed in Experiment 1, but a disadvantage should be observed in Experiment 2. Our participants learned about the added discrimination and generally showed the effects predicted by the comparator hypothesis.     

Latent inhibition as a performance deficit resulting from CS—context associations

Treatments that attenuate latent inhibition (LI) were examined using conditioned suppression in rats. In Experiment 1, retarded conditioned responding was produced by nonreinforced exposure to the CS prior to the CS-US pairings used to assess retardation (i.e., conventional LI). In Experiment la, retarded conditioned responding was induced by preexposure to pairings of the CS and a weak US prior to retardation-test pairings of the CS with a strong US (i.e., Hall-Pearce [1979] LI). Both types of LI were attenuated by extensive exposure to the training context (i.e., context extinction) following the CS-US pairings of the retardation test. Experiment 2 examined the specificity of the attenuated LI effect observed in Experiment 1. After preexposure to two different CSs in two different contexts, each CS was paired with a US in its respective preexposure context. One of the two contexts was then extinguished. This attenuated LI to a greater degree for the CS that had been trained in the extinguished context. Experiment 3 differentiated the roles in LI of CS-context associations and context-US associations. Following preexposure to the CS in the training context, LI was reduced by further exposure to the CS outside the training context. This observation was interpreted as implicating the CS-context association as a factor in LI. Thus, the results of these experiments suggest that LI is a performance deficit mediated by unusually strong CS-context associations. Implications for Wagner’s (1981) SOP model and Miller and Matzel’s (1988) comparator hypothesis are discussed.     

Divergence of conditioned eyeblink and conditioned fear in backward Pavlovian training

Two experiments of Pavlovian conditioning with rabbits evaluated the effects of initiating or continuing a conditioned stimulus (CS) after a paraorbital unconditioned stimulus (US). In Experiment 1, backward pairings, in which a CS came on after the US, produced a CS that appeared inhibitory on a measure of eyeblink conditioning but excitatory on a potentiated-startle measure of conditioned fear. In Experiment 2, extending the duration of a CS that came on prior to the US, so that it continued after the US, decreased eyeblink conditioned responses, whereas it increased conditioned fear. The data from the two experiments confirm and extend those of Tait and Saladin (1986), supporting the suppositions of AESOP (Wagner & Brandon, 1989) that conditioned eyeblink and conditioned fear can be dissociated under various temporal relationships between the CS and US.     

Integration of spatial relationships and temporal relationships in humans

Three experiments tested human participants on a two-dimensional, computer, landmark-based search task to assess the integration of independently acquired spatial and temporal relationships. Experiment 1 showed that A-B spatial training followed by B-outcome spatial training resulted in spatial integration in such a way that A was effectively associated with the outcome. Experiment 2 showed that A-B spatial and temporal training followed by B-outcome spatial and temporal training resulted in integration that created both spatial and temporal relationships between A and the outcome. Experiment 3 refuted an alternative explanation, one that is based on decision-making speed, to the temporal-integration strategy that was suggested by Experiment 2. These results replicate in humans the observations regarding spatial integration made by Sawa, Leising, and Blaisdell (2005) using a spatial-search task with pigeons, and they extend those observations to temporal integration.     

Outcome-specific conditioned inhibition in Pavlovian backward conditioning

In the present experiments, the outcome specificity of learning was explored in an appetitive Pavlovian backward conditioning procedure with rats. The rats initially were administered Pavlovian backward training with two qualitatively different unconditioned stimulus conditioned-stimulus (US-CS) pairs of stimuli (e.g., pellet --> noise or sucrose --> light), and then the effects of this training were assessed in Pavlovian-to-instrumental transfer (Experiment 1) and retardation-of-learning (Experiment 2) tests. In the transfer test, it was shown that during the last 10-sec interval, the CSs selectively reduced the rate of the instrumental responses with which they shared a US, relative to the instrumental responses with which they did not share a US. The opposite result was obtained when the USs (in the absence of the CSs) were presented noncontingently. In the retardation test, conditioned magazine approach, responding to the CSs was acquired more slowly when the stimulus-outcome combinations in the backward and the forward conditioning phases were the same, as compared with when they were reversed. These results are collectively in accord with the view that Pavlovian backward conditioning can result in the formation of outcome-specific inhibitory associations. Alternative views of backward conditioning are also examined.     

Reminder-induced attenuation of the effect of relative stimulus validity

The roles of deficient acquisition and deficient expression of learned information in the effect of relative stimulus validity were examined using rats in a conditioned lick suppression paradigm. Recovery from the effect without further pairings of the conditioned stimulus (CS) and the unconditioned stimulus (US) would favor an interpretation of the relative validity effect based on a latent CS-US association as distinct from a failure to acquire the CS-US association. As a potential recovery manipulation, “reminder” treatments, consisting of the US alone (Experiment 1) or the CS alone (Experiment 2), were administered following relative validity training. In both cases, subjects for which the CS target was of low relative predictive validity exhibited enhanced responding relative to appropriate controls. Additionally, Experiment 2 showed that the amelioration of the relative validity deficit was stimulus specific. Thus, the results of these experiments support previous suggestions that the performance deficit resulting from low relative stimulus validity is due, at least in part, to a failure to express acquired information (Cole, Barnet, & Miller, 1995a).     

Development of excitatory backward associations during the establishment of forward associations in a delayed conditional discrimination by pigeons

The development of excitatory backward associations in pigeons was demonstrated in three experiments involving conditional discriminations with differential outcomes. In Phase 1 of all three experiments, correct comparison choices following one sample were followed by food, whereas correct comparison choices following the other sample were followed by presentation of an empty feeder. In Phase 2, the food and no-food events that served as outcomes in Phase 1 replaced the samples. When the associations tested in Phase 2 were consistent with the comparison-outcome associations developed in Phase 1, transfer performance was significantly better than when the Phase 2 associations were inconsistent with the Phase 1 associations. In Experiment 1, an identity matching-to-sample task was used with red and green samples and red and green comparisons. In Experiment 2, a symbolic matching task was used with shape samples and hue comparisons, and it was shown that the backward associations formed were between the trial outcome (food or no food) and the correct comparison. In Experiment 3, it was determined that the transfer effects observed in these experiments did not depend on either the similarity of behavior directed toward the samples in the training and test phases, or the similarity of food and no-foodexpectancies generated by the samples in Phase 1 to food and no-foodevents presented as samples in Phase 2.     

CS-US temporal relations in blocking

In four trace-conditioning experiments with rats, the influence on the blocking of differences between the blocking cue-unconditioned stimulus (US) and the blocked cue-US trace intervals was explored. Experiment 1 demonstrated blocking despite the blocked cue’s having a shorter trace interval than the blocking cue in both elemental (Phase 1) and compound (Phase 2) training. In Experiment 2, blocking was attenuated when the blocked cue had a longer trace interval than did the blocking cue in both elemental and compound training. In Experiments 3 and 4, the trace intervals of the two cues during compound training were matched (i.e., unlike in Experiments 1 and 2, neither had temporal priority). Blocking was attenuated when the blocking cue trace interval in the elemental phase was shorter (Experiment 3) or longer (Experiment 4) than the compound cue trace during compound training. The findings indicate that subjects encode interstimulus intervals, and they further suggest that cue competition is greatest when the competing cues have the same temporal information as the US.     

Overshadowing of explicitly unpaired conditioned inhibition is disrupted by preexposure to the overshadowed inhibitor

In two conditioned lick-suppression experiments with rats, the interaction of preexposure to a target stimulus and subsequent overshadowing of conditioned inhibition treatment was examined. Blaisdell, Bristol, Gunther, and Miller (1998) have demonstrated that stimulus preexposure and overshadowing counteract each other in their effects on Pavlovian excitation, producing strong excitatory responding to the target stimulus. In the present experiments, a conditioned inhibition analogue of this effect was examined. Overshadowing of conditioned inhibition (i.e., attenuation of inhibitory control of behavior by the target stimulus) was demonstrated when a more salient stimulus was compounded with the target inhibitor during conditioned inhibition training. However, the overshadowing deficit was attenuated by preexposing the target stimulus prior to overshadowing treatment. To account for this phenomenon, we contrast the comparator hypothesis (Miller & Matzel, 1988) with contemporary models that focus on associative acquisition.     

Recovery of conditioned suppression after backward pairings

In four conditioned suppression experiments with rats (Rattus norvegicus), backward pairings of a shock unconditioned stimulus (US) and a tone conditioned stimulus (CS) eliminated an already established conditioned response (CR), but there was recovery of the CR if the shock was later withheld. In Experiment 1, there was recovery after backward pairings, regardless of whether the period after the US was normally shock free or not. In Experiment 2, the occurrence of recovery depended on the CS’s being presented closely after the US in response elimination. Levels of recovery were positively correlated with the resistance of the response to elimination during backward pairings (Experiments 3 and 4). Taken together, these data support the notion that recovery after backward pairings is a form of renewal (see, e.g., Bouton, 1991) and is not due toprotection from extinction.     

Pavlovian conditioning in multiple contexts: Competition between contexts for comparator status

Water-deprived rats were used to investigate the effects of training a CS in more than one context on conditioned lick suppression. In each experiment, partial reinforcement of the CS was intermingled with unsignaled presentations of the US. In Experiment 1, subjects were either trained in one context alone, trained consecutively in two contexts (such that all training in one context occurred prior to any training in the second context), or trained alternately in two contexts. Following training, the first context, the second context, or neither context was extinguished. Testing of the CS occurred in a third (neutral) context. To the extent that either training context became established as a comparator stimulus for the CS, the comparator hypothesis (Miller & Matzel, 1988) predicts an increase in excitatory responding to the CS following extinction of that context. Subjects trained in a single context exhibited appreciable fear of the CS only when the CS’s training context had been extinguished. Additionally, subjects trained consecutively in the two contexts showed increased fear of the CS following extinction of the second, but not the first training context (i.e., a recency effect). Subjects trained alternately in the two contexts showed no increased fear of the CS as a result of either context alone being extinguished. In Experiment 2, subjects trained alternately in two contexts showed increased fear of the CS only when both training contexts were extinguished, suggesting that both training contexts had become comparator stimuli. These data indicate that multiple training contexts can either compete or act synergistic-ally in modulating responding to a Pavlovian trained CS as a function of the order of training in the different contexts.     

Recovery of the rabbit’s conditioned nictitating membrane response without direct reinforcement after extinction

Three experiments demonstrated that, following the extinction of an established conditioned stimulus (CSA—e.g., tone), the pairing of a novel, cross-modal stimulus (CSB—e.g., light) with the unconditioned stimulus (US) results in strong recovery of responding to the extinguished CSA. Experiment 1 demonstrated that the recovery of responding to CSA is not the result of US reinstatement but is attributable to pairings of CSB with the US. Experiment 2 demonstrated that the recovery of responding is specific to CSA and is not the result of cross-modal generalization. Experiment 3 revealed that a large number of CSB-US pairings in Stage 1 significantly reduced the amount of recovery to CSA during subsequent CSB-US trials. Experiment 3 also provided unexpected evidence of cross-modal secondary extinction. The extinction and subsequent recovery of responding seen in the present experiments is discussed with respect to possible contributions from contextual associations, CS processing, US processing, conditioned response expression, and layered excitatory associations.     

Overshadowing as a function of trial number: Dynamics of first- and second-order comparator effects

In two conditioned lick suppression experiments with rats, we examined the permanence of the overshadowing effect as a function of the number of compound reinforced training trials. In Experiment 1, robust overshadowing was observed following 4 compound-US pairings but dissipated with 36 pairings. Overshadowing decreased because responding to the overshadowed stimulus increased, not because responding by the control group decreased. This dissipation was stimulus specific and not attributable to a response ceiling. Experiment 2 extended the generality of the effect to a sensory preconditioning design and further demonstrated that overshadowing lost through many compound-US pairings was restored by posttraining extinction of the training context. The results are explicable in terms of the extended comparator hypothesis (Denniston, Savastano, & Miller, 2001) under the assumption that the impacts of first- and second-order comparator processes grow differentially as a function of number of trials.     

The dual role of the context in postpeak performance decrements resulting from extended training

The context??s role in Pavlovian conditioning depends on the trial spacing during training, with massed trials revealing a function akin to that of discrete stimuli, and spaced trials revealing a modulatory function (Urcelay & Miller, Journal of Experimental Psychology. Animal Behavior Processes, 36, 268?C280, 2010). Here we examined the contextual determinants of a common but largely ignored effect: attenuated conditioned responding with extended reinforced training (i.e., a postpeak performance deficit [PPD]). Contextual sources of PPDs were investigated in four fear-conditioning experiments with rats. In Experiment 1, as the number of reinforced trials increased, conditioned responding decreased, even when testing occurred outside the training context. Experiment 2 revealed opposing influences of context on the PPD based on trial spacing, which interacted with whether testing occurred in the training context. This finding reconciles Experiment 1??s results with previous data (Bouton, Frohardt, Sunsay, Waddell, & Morris, Journal of Experimental Psychology. Animal Behavior Processes, 34, 223?C236, 2008). Experiment 3 suggested that extended training with these parameters did not lead to habituation to conditioned or unconditioned stimuli. In Experiment 4, few or many massed training trials were followed orthogonally by context extinction or no context extinction. After many pairings, context extinction reduced the PPD (i.e., enhanced responding), suggesting a competitive role of the context. These results, together with prior data suggesting that context modulates expressions of the PPD, are consistent with the view that contexts can play two distinctly different roles.