Posttrial effects of presenting vs. omitting expected shock USs in the conditioned suppression procedure: Concurrent measurement of barpress suppression and freezing

Barpress suppression in a 1-min interval following CS trials was investigated using 16 rats in a conditioned suppression procedure with a two-stage design. For one group, each CS co-terminated with a brief shock US in Stage 1; then, in Stage 2, only half the CSs ended with a shock, which in turn was followed 1 min later by a second shock. For a second group, the two stages were reversed. When CSs were followed by single shocks in Stage 1, posttrial suppression weakened across trials; but when, in Stage 2, double shocks followed half the CSs, posttrial suppression grew stronger. When half the trials were followed by double shocks in Stage 1, posttrial suppression was maintained at initial levels but weakened in Stage 2 when single shocks followed each trial. In both stages, posttrial suppression was stronger on nonreinforced than on reinforced trials. Two factors were hypothesized to control posttrial suppression. First, posttrial suppression weakens with training under the single-shock procedure because post-shock temporal stimuli come to inhibit fear unless themselves paired with shock. Second, posttrial suppression is stronger on nonreinforced trials than on reinforced trials because freezing behaviors initiated during the CS are not disrupted by a US and so persist into the posttrial interval.     

CS modality effects in one-trial backward and forward excitatory conditioning as assessed by conditioned suppression of licking in rats

Rats received a single 4-sec 1-mA grid-shock US either preceded or followed by a 4-sec tone or light CS. Conditioning was later assessed by comparing the amount of lick suppression evoked by the forward- or backward-paired CS versus an explicitly unpaired CS. The backward-paired CS produced more suppression than the unpaired CS only when both were tone; the light evoked strong suppression whether paired or not. In the forward procedure, tone produced more suppression when paired and less when unpaired than did light; conditioning thus appeared stronger with the tone. In one experiment, observations showed that rats froze during the forward-paired tone but not during the light. Increasing CS duration from 4 to 12 sec had no effect for the forward-paired light but increased freezing to the forward-paired tone. Another experiment showed similar unconditioned suppression to tone and light but faster habituation to tone. Problems that these results create for interpreting evidence for excitatory backward conditioning in the conditioned suppression procedure are discussed.     

One-trial simultaneous and backward excitatory fear conditioning in rats: Lick suppression, freezing, and rearing to CS compounds and their elements

Three experiments with rat subjects sought to enhance one-trial excitatory simultaneous and backward fear conditioning by using a two-element compound conditioned stimulus (CS) instead of only a single element. During conditioning, experimental groups received a 4-sec CS either coextensively with a 1-mA grid-shock unconditioned stimulus (US) or immediately after US termination. In subsequent tests, CSs evoked more lick suppression and freezing in these groups than in various controls. Compound CSs evoked more lick suppression and freezing than did CS elements, but did so equally for experimental and control groups. Therefore, the use of compounds did not enhance conditioning. Unexpectedly, an explicitly unpaired control in which CS followed US termination by 3 min tended to show more CS-evoked suppression and freezing than did a control in which CS preceded US onset by 3 min. This result raises the possibility that associations between the CS and the training context might engender responding to backward-paired CSs.     

One-trial excitatory backward conditioning as assessed by conditioned suppression of licking in rats: Concurrent observations of lick suppression and defensive behaviors

Twenty-eight male albino rats were given a single 4-sec 1-mA electric-grid-shock unconditioned stimulus (US). In the same session they received two 12-sec conditioned stimuli (CSs). One CS (explicitly unpaired) terminated 180 sec before the US began; the other (backward paired) began immediately after the US terminated. The CSs used were a 1000-Hz 85-dB tone and an 84-dB click; their roles were counterbalanced. Over the next 2 days, each CS was presented for 2 min while the rats drank from a water bottle. The backward-paired CS was found to suppress licking more than the explicitly unpaired CS. This suppression was accompanied by an increase in defensive behavior (freezing and freeze/nod) and by a decrease in other activity. The suppression did not seem to be due to a maintained or enhanced CS-orienting response reflex, nor could it be attributed to an adventitiously reinforced interfering operant. The results support the presumption made in previous reports that the lick suppression evoked by a backward CS reflected one-trial backward excitatory fear conditioning.     

CS modality,context conditioning,and conditioned freezing

Two studies used a one-trial-a-day aversive conditioning procedure with rats as subjects to investigate the effects of a noise versus a light CS on conditioned freezing. Experiment 1 demonstrated that less conditioned freezing was elicited by the light, although the two CSs led to similar levels of freezing to the contextual cues of the conditioning chamber. Experiment 2 replicated these outcomes and showed that the manipulation of CS intensity produced results similar to those of modality, with the more intense CSs eliciting less freezing. The second experiment also determined that freezing to contextual cues resulted from context conditioning. According to the Rescorla-Wagner model, CSs that condition poorly should generate little competition with context conditioning. Since neither the modality nor intensity factor reliably influenced context conditioning, as measured by context-evoked freezing, the studies provide no support for the view that the effects on CS-evoked freezing represent differences in the strength of conditioning to the various stimuli. This finding raises the possibility that all of the CSs conditioned well but varied in their abilities to elicit freezing because they differed in terms of the form of defensive behavior under their control.     

Pre-exposure enhances recovery of conditioned responding after extinction

Four experiments used a within-subjects design with rats to study the effects of preexposure on the restoration of fear responses (freezing) to an extinguished conditioned stimulus (CS). In each experiment, rats were preexposed to one CS (A), but not to another (B), and then were exposed to pairings of each of these CSs with an aversive unconditioned stimulus (US). In each experiment, there was less freezing to A than to B across extinction, showing a latent inhibitory effect of preexposure. There was no differential recovery to A and B following either a US reexposure (Experiment 1) or a delay interval (Experiment 2). However, when a delay interval included US reexposure, there was greater recovery to the preexposed CS, A, than to the nonpreexposed CS, B (Experiments 1, 3, and 4). These results suggest that the effects of US reexposure and delay combine to affect recovery from the depressive effects of CS-alone exposure. The results are consistent with the view that US reexposure produces better mediated conditioning of CSs that are strongly associated with the context. The results may additionally reflect an effect of preexposure on the learning produced by extinction.     

Trial spacing effects in pavlovian conditioning: A role for local context

Two conditioned lick-suppression experiments with rats were conducted in order to replicate and extend findings by Ewing, Larew, and Wagner (1985). Ewing et al. observed that excitatory responding to a CS paired with a footshock US was attenuated when the ITIs thatpreceded each CS-US trial were short (60 sec) relative to when they were long (600 sec). This effect was isolated in the influence of the preceding ITI because the preceding ITI was consistently short for one CS and consistently long for a different CS, while the following ITIs were equally often short and long for both CSs. Ewing et al. interpreted this finding in the framework of Wagner’s (1981) SOP model. Experiment 1 replicated this trial-spacing effect and demonstrated a similar effect under conditions in which thefollowing ITI was consistently short for one CS and consistently long for a different CS, while the durations of preceding ITIs were equally often short and long for both CSs. Experiment 2 revealed that the detrimental effect of a short preceding or a short following ITI could be alleviated by extinguishing the conditioning context after CS-US training. The latter observation indicates that the trial-spacing effect is not mediated by a failure of a CS trained with a short ITI to enter into excitatory associations with the US, a conclusion that is not wholly consistent with the SOP model. Finally, we suggest that short pretrial and short posttrial ITIs may enhance the excitatory value of local context cues that modulate responding to a CS.     

Stimulus specificity of concurrent recovery in the rabbit nictitating membrane response

Three experiments demonstrated that, following the extinction of an established conditioned stimulus (CS; e.g., tone), the pairing of an orthogonal stimulus from another modality (e.g., light) with the unconditioned stimulus (US) results in strong recovery of responding to the extinguished CS. This recovery occurred to about an equal degree regardless of whether or not initial training contained unambiguous stimulus—reinforcer relationships—that is, consistent CS—US pairings—or some degree of ambiguity, including intramodal discrimination training, partial reinforcement, or even cross-modal discrimination training (tone vs. light). Experiments 1 and 2 demonstrated that this recovery of responding was largely specific to the extinguished CS, but moderate generalization to other stimuli from the same modality did appear. The results are discussed with reference to alternative mechanisms applicable to learning-dependent generalization between otherwise distinct CSs. These models assume that such generalization is mediated by either a shared response, shared reinforcer, shared context, or shared hidden units within a layered neural network. A specific layered network is proposed to explain the present results as well as other types of savings seen previously in conditioning of the rabbit nictitating membrane response.     

Bidirectional heart rate responses in rats associated with excitatory and inhibitory stimuli

Following classical conditioning to a shock-reinforced tone CS (T₁+), heart rate (HR) of three groups of rats was examined in response to a new reinforced tone (T₂+) and a nonreinforced light (L?) CS given during conditioned inhibition (T₂+ vs. T₁L?), discrimination conditioning (T₂+ vs. L?), or explicitly unpaired (T₂/L? vs. US alone) procedures. Decelerative HR reactions occurred to the reinforced T₂+ and T₂+ CSs. To the respective nonreinforced CSs, the conditioned inhibition group displayed diminished but sizable HR deceleration, the discrimination group showed near-zero responding, and the explicitly upaired group showed HR acceleration. Subsequent reversal conditioning to L was retarded in the conditioned inhibition and explicitly unpaired groups relative to the discrimination group. Group differences on combined-cue [T₂/L?) trials were not found. Both the HR responses during inhibitory training and the reversal-conditioning impairments suggest that inhibition may have been established to L? in the conditioned inhibition and explicitly unpaired groups.     

General transfer across sensory modalities survives reductions in the original conditioned reflex in the rabbit

Two experiments demonstrated that transfer of training between CSs from different sensory modalities survived substantial reductions in responding to the first CS. In both experiments, animals received three stages of training. Stage 1 entailed CS-US training with a CS from one modality (e.g., light), and Stage 3 entailed CS-US training with a CS from another modality (e.g., tone). The experiments differed in treatment during Stage 2. In Experiment 1, animals either remained in their home cages or received unreinforced exposures to the first CS, which extinguished the original CR. In Experiment 2, the animals received either continued CS-US training or exposure to the CS and US but at a long interval (2,800 msec), which eliminated the original CR. As the baseline for detection of transfer effects, each experimental group had a control group that received Stage 1 training with a 2,800-msec CS-US interval, which produced minimal CR acquisition. The results of both experiments revealed substantial positive transfer across CS modalities regardless of the treatment during Stage 2. The transfer did not appear immediately on test presentations of the second CS in Stage 3. Rather, the transfer appeared as an enhancement in the rate of CR acquisition after reinforced training with the second CS had commenced. The results are discussed with respect to stimulus generalization, neutralization of background stimuli, and learning processes superordinate to specific associations.     

Surprise and blocking: Effects of the number of compound trials

In an experiment on conditioned suppression of licking in thirsty rats, subjects received either one or two trials to a tone-light compound, either preceded or not preceded by four conditioning trials to the light alone. Prior conditioning to the light blocked conditioning to the tone in subjects receiving two compound trials but not in those receiving only one compound trial. The blocking observed in the two-trial groups was abolished either by the addition of an unexpected second posttrial shock 10 sec after the first on each compound trial or by the omission of an expected second, posttrial shock. The comparable operations had no effect on conditioning to the tone in the one-trial group. In this preparation, both blocking and the attenuation of blocking by surprising changes in reinforcement appear to require more than one trial to appear.     

Transfer across CS-US intervals and sensory modalities in classical conditioning of the rabbit

Two experiments investigated transfer of the rabbit’s conditioned nictitating membrane response (NMR) from shorter to longer CS-US intervals in conjunction with a change in CS modality, for example, light to tone. In Experiment 1, three experimental groups received initial training with a 400-msec CS-US interval, which produced substantial CR acquisition, and three control groups received initial training with a 2,800-msec CS-US interval, which produced minimal CR acquisition. Subsequently, the experimental and control groups received training with an 800-, 1,800-, or 2,800-msec CS-US trace interval. At the same time, the modality of the CS was changed from tone to light (or vice versa). Experiment 2 contained three groups that received initial exposure to a 400-msec CS-US interval, a 2,800-msec CS-US interval, or just the experimental chambers. Subsequently, all three groups received training with an 800-msec CS-US interval in a different CS modality. The results of both experiments revealed substantial positive transfer across CS modalities from the 400-msec CS-US interval to the 800-msec CS-US interval. There was also significant transfer to the 1,800-msec but not the 2,800-msec CS-US interval. The transfer did not appear immediately on test presentations of the second CS. Rather, the transfer appeared as an enhancement in the rate of CR acquisition after reinforced training with the second CS had commenced. The results are discussed with respect to mechanisms of transfer and facilitation of trace conditioning.     

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.     

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).     

Overshadowing and CS duration: counteraction and a reexamination of the role of within-compound associations in cue competition

In the present experiments, we examined the role of within-compound associations in the interaction of the overshadowing procedure with conditioned stimulus (CS) duration, using a conditioned suppression procedure with rats. In Experiment 1, we found that, with elemental reinforced training, conditioned suppression to the target stimulus decreased as CS duration increased (i.e., the CS duration effect), whereas, with compound reinforced training (i.e., the overshadowing procedure), conditioned suppression to the target stimulus increased as CS duration increased. In subsequent experiments, we replicated these findings with sensory preconditioning and demonstrated that extinction of the overshadowing stimulus results in retrospective revaluation with short CSs and in mediated extinction with long CSs. These results highlight the role of the duration of the stimulus in behavioral control. Moreover, these results illuminate one cause (the CS duration) of whether retrospective revaluation or mediated extinction will be observed.     

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.     

One-trial simultaneous and backward fear conditioning as reflected in conditioned suppression of licking in rats

In three experiments, groups of albino rats received one strictly simultaneous pairing of a 4-sec auditory conditioned stimulus (CS) and a 4-sec 1-mA shock unconditioned stimulus (US). Other groups received a backward pairing, in which the US began before the CS, or a forward pairing, in which the CS began before the US. Control groups received only the US or received both the CS and the US but widely separated in time. Later, the CS was presented while the rats licked a drinking tube for water, and CS-elicited suppression of licking was taken as an index of the Pavlovian conditioned response (CR). It was found that groups receiving a single forward or a single simultaneous pairing suppressed more than groups that had received a backward pairing; and the backward groups, in turn, suppressed more than the control groups. It appears, then, that excitatory fear conditioning, as reflected in conditioned suppression of licking in rats, can be produced in a single trial by both backward and simultaneous conditioning procedures.     

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).     

Enhancement of conditioned inhibition via an extinction treatment

Rats were used in a conditioned-suppression paradigm to determine whether an extinction treatment would enhance a moderately developed conditioned inhibitor (CS?). To dissipate unconditioned suppression to the training stimuli, the subjects were first habituated to the stimuli and then given Pavlovian conditioned-inhibition (CI) training involving reinforced presentations of a clicker and nonreinforced compound presentations of that stimulus and the intended CS?, either a light or a tone. Thereafter, experimental subjects received presentations of their CS? by itself, whereas controls received no further training. Following the occurrence and loss of conditioned suppression to the CS? in the extinction phase, summation and retardation tests showed enhanced CI for the experimental subjects relative to both the controls and their own earlier levels of inhibitory performance. In fact, the enhanced inhibition for the experimental subjects approximated that shown by a comparison group for which the CS? had been strongly developed as an inhibitor. These findings suggest that an excitatory representation is associated with the CS? early in CI training, and that subsequent presentations of the CS? by itself strengthen its inhibitory effect by allowing it to be nonreinforced in the presence of that representation.     

Forgetting of a CS attribute in a conditioned suppression paradigm

Although a number of studies have demonstrated nearly complete retention of fear in a conditioned suppression task, they provide little information about the nature of the memory for the CS. The purpose of the present experiment was to investigate the retention of an attribute of a tonal CS that had been paired with shock and was thus capable of eliciting a conditioned emotional response (CER) in rats. The Kamin blocking effect was utilized to detect changes in the memory of CS attributes. Either 1 or 21 days following conditioning to a tone, separate groups of rats received compound conditioning in which either the original or a novel tone was combined with a light. Subsequent measurement of suppression to the added element (light) indicated that only the original CS produced blocking at the short delay, but that both original and novel tones resulted in blocking at the 21-day interval. This increase in the extent of blocking suggests that memory for specific attributes of the CS does diminish as a function of time.