The role of temporal variables in inhibition produced through extinction

In two experiments with rats as subjects, the temporal characteristics of inhibition produced through extinction were investigated. Each experiment established two independent signals for unconditioned stimulus presentation, one trace and one delay. Following initial training, either the trace or the delay conditioned stimulus (CS) was massively extinguished. In Experiment 1, a summation test established that an extinguished delay CS (but not a neutral CS) passed a summation test with a delay, but not with a trace, transfer excitor, and an extinguished trace CS (but not a neutral CS) passed a summation test with a trace, but not with a delay, transfer excitor. In Experiment 2, a retardation test showed retarded behavioral control by an extinguished delay CS when the CS was retrained as a delay CS, but not as a trace CS, and by an extinguished trace CS when the CS was retrained as a trace CS, but not as a delay CS. The results are discussed in terms of contemporary theories of extinction.     

Temporal encoding in trace conditioning

Conditioned lick suppression in rats was used to explore the role of timing in trace conditioning. In Experiment 1, two groups of rats were exposed to pairings of a CS (CS1) with a US, under conditions in which the interstimulus interval (ISI) that separated CS1 offset and US onset was either 0 or 5 sec. Two additional groups were also exposed to the same CS1→US pairings with either a 0 or a 5-sec ISI, and then received “backward” second-order conditioning in which CS1 was immediately followed by a novel CS2 (i.e., CS1→CS2). A trace conditioning deficit was observed in that the CS1 conditioned with the 5-sec gap supported less excitatory responding than the CS1 conditioned with the 0-sec gap. However, CS2 elicited more conditioned responding in the group trained with the 5-sec CS1-US gap than in the group trained with the 0-sec CS1-US gap. Thus, the CS1-US interval had inverse effects on first- and second-order conditioned responding. Experiment 2 was conducted as a sensory preconditioning analogue to Experiment 1. In Experiment 2, rats received the CS1?CS2 pairings prior to the CS1→US pairings (in which CS1 was again conditioned with either a 0 or a 5-sec ISI). Experiment 2 showed a dissociation between first- and second-order conditioned responding similar to that observed in Experiment 1. These outcomes are not compatible with the view that differences in responding to CSs conditioned with different ISIs are mediated exclusively by differences in associative value. The results are discussed in the framework of the temporal coding hypothesis, according to which temporal relationships between events are encoded in elementary associations.     

Temporal integration and instrumental conditioned reinforcement

Stimuli associated with primary reinforcement for instrumental behavior are widely believed to acquire the capacity to function as conditioned reinforcers via Pavlovian conditioning. Some Pavlovian conditioning studies suggest that animals learn the important temporal relations between stimuli and integrate such temporal information over separate experiences to form a temporal map. The present experiment examined whether Pavlovian conditioning can establish a positive instrumental conditioned reinforcer through such temporal integration. Two groups of rats received either delay or trace appetitive conditioning in which a neutral stimulus predicted response-independent food deliveries (CS1→US). Both groups then experienced one session of backward second-order conditioning of the training CS1 and a novel CS2 (CS1–CS2 pairing). Finally, the ability of CS2 to function as a conditioned reinforcer for a new instrumental response (leverpressing) was assessed. Consistent with the previous demonstrations of temporal integration in fear conditioning, a CS2 previously trained in a trace-conditioning protocol served as a better instrumental conditioned reinforcer after backward second-order conditioning than did a CS2 previously trained in a delay protocol. These results suggest that an instrumental conditioned reinforcer can be established via temporal integration and raise challenges for existing quantitative accounts of instrumental conditioned reinforcement.     

Retardation of conditioned excitation following operational inhibitory blocking

Water-deprived adult rats were used in a conditioned-suppression-of-licking procedure to determine the effect of inhibitory training with a novel stimulus trained in simultaneous compound with a previously established conditioned inhibitor. This procedure constitutes an inhibitory analogue to the excitatory blocking procedure in classical conditioning. The conditioned-inhibition training consisted of either explicitly unpaired CS and US presentations or negative contingency training, in which the likelihood of the US was greater in the absence than in the presence of the CS, but the CS and the US were occasionally paired. To assess conditioned inhibition, a retardation test was used, and comparable retardation was obtained for subjects that were administered the blocking treatment and control subjects given similar conditioned-inhibition training with a compound stimulus in which the nontarget element was not previously established as a conditioned inhibitor.     

Intertrial unconditioned stimuli differentially impact trace conditioning

Three experiments assessed how appetitive conditioning in rats changes over the duration of a trace conditioned stimulus (CS) when unsignaled unconditioned stimuli (USs) are introduced into the intertrial interval. In Experiment 1, a target US occurred at a fixed time either shortly before (embedded), shortly after (trace), or at the same time (delay) as the offset of a 120-s CS. During the CS, responding was most suppressed by intertrial USs in the trace group, less so in the delay group, and least in the embedded group. Unreinforced probe trials revealed a bell-shaped curve centered on the normal US arrival time during the trace interval, suggesting that temporally specific learning occurred both with and without intertrial USs. Experiments 2a and 2b confirmed that the bulk of the trace CS became inhibitory when intertrial USs were scheduled, as measured by summation and retardation tests, even though CS offset evoked a temporally precise conditioned response. Thus, an inhibitory CS may give rise to new stimuli specifically linked to its termination, which are excitatory. A modification to the microstimulus temporal difference model is offered to account for the data.     

Explaining the effects of relative time in trace conditioning: A preliminary test of a comparator hypothesis

Scalar expectancy theory (SET) predicts that postacquisition manipulations of background expectancy should alter conditioned performance. An experiment was performed to test the application of this hypothesis to an explanation of the “temporal context” effect in trace conditioning. Pigeons were trained on an inhibitory trace conditioning procedure and then subjected to postacquisition manipulations of background expectancy. Nonreinforced exposure to the training apparatus eliminated conditioned withdrawal, exposure to USs under very long interreinforcer intervals slightly weakened conditioned withdrawal, and home-cage confinement had no effect on conditioned withdrawal. These results are discussed in terms of the predictions of SET and the role of background excitation in conditioned inhibition.     

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).     

Blocking with serial and simultaneous compounds in a trace conditioning procedure

Blocking of conditioned suppression in rats was studied in three experiments using serial and simultaneous compounds in Pavlovian trace conditioning procedures. Experimental groups were first given trace conditioning trials with a 2-sec stimulus (A) presented at least 60 sec before an electric grid shock US. Next, both experimental and control groups received reinforced trials with a compound stimulus (AB). Both A and B were 2 sec in duration and were presented at least 60 sec before the US. For some groups during AB training, the A stimulus preceded the B stimulus; for others, B preceded A; for still others, A and B occurred simultaneously. Conditioning was subsequently assessed separately to both A and B. The results were as follows: First, varying the interval between the onset of A and the US during A training appeared to produce significantly different levels of conditioning to A but did not detectably affect A’s ability to block conditioning to B. Second, blocking was observed in both simultaneous and serial procedures. Third, in the serial procedure, A blocked conditioning to B whether it preceded B or followed B in the AB compound. Fourth, in tests given after AB conditioning, the experimental and control groups suppressed similarly to A. The relevance of these results to the conditioning model of Rescorla and Wagner (1972) and to Mackintosh’s (1975b) theory of attention are discussed.     

Trial number and compound stimuli temporal relationship as joint determinants of second-order conditioning and conditioned inhibition

Two conditioned lick suppression experiments with rats used feature-negative training (A-footshock trials intermixed with nonreinforced XA presentations) to analyze the role of the number of XA compound presentations and the temporal relationship of the elements within the compound (simultaneous or serial) as determinants of the resulting behavioral control. Second-order conditioning (i.e., excitatory behavioral control by X) was observed to decline as the number of XA compound trials was increased. This decline was more rapid if X and A were presented simultaneously, as opposed to serially (i.e., X before A; Experiment 1). Conditioned inhibition to X, as assessed by a summation test (Experiment 1) and a retardation test (Experiment 2), increased with the number of XA trials and did so more quickly for simultaneous than for serial pairings of X and A. The results help to clarify previously discrepant findings regarding factors that promote excitation versus inhibition with this protocol.     

Proactive interference by cues presented without outcomes: Differences in context specificity of latent inhibition and conditioned inhibition

This report is part of a larger project examining associative interference as a function of the nature of the interfering and target associations. Lick suppression experiments with rats assessed the effects of context shifts on proactive outcome interference by latent inhibition (LI) and Pavlovian conditioned inhibition (CI) treatments on subsequently trained Pavlovian conditioned excitation treatment. LI and CI were trained in Context A during Phase 1, and then excitation treatment was administered in Context B during Phase 2, followed by tests for conditioned excitation in Contexts A, B, or C. Experiment 1 preliminarily established our LI and CI treatments and resulted in equally retarded acquisition of behavioral control when the target cue was subsequently trained as a conditioned excitor and tested in Context A. However, only CI treatment caused the target to pass a summation test for inhibition. Centrally, Experiment 2 consisted of LI and CI treatments in Context A followed by excitatory training in Context B. Testing found low excitatory control by both LI and CI cues in Context A relative to strong excitatory control in Context B, but CI treatment transferred to Context C more strongly than LI treatment. Experiment 3 determined that LI treatment failed to transfer to Context C even when the number of LI trials was greatly increased. Thus, first-learned LI appears to be relatively context specific, whereas first-learned CI generalizes to a neutral context. These observations add to existing evidence that LI and CI treatments result in different types of learning that diverge sharply in transfer to a novel test context.     

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.     

Extinction with multiple excitors

Four conditioned suppression experiments with rats, using an ABC renewal design, investigated the effects of compounding the target conditioned excitor with additional, nontarget conditioned excitors during extinction. Experiment 1 showed stronger extinction, as evidenced by less renewal, when the target excitor was extinguished in compound with a second excitor, relative to when it was extinguished with associatively neutral stimuli. Critically, this deepened extinction effect was attenuated (i.e., more renewal occurred) when a third excitor was added during extinction training. This novel demonstration contradicts the predictions of associative learning models based on total error reduction, but it is explicable in terms of a counteraction effect within the framework of the extended comparator hypothesis. The attenuated deepened extinction effect was replicated in Experiments 2a and 3, which also showed that pretraining consisting of weakening the association between the two additional excitors (Experiments 2a and 2b) or weakening the association between one of the additional excitors and the unconditioned stimulus (Experiment 3) attenuated the counteraction effect, thereby resulting in a decrease in responding to the target excitor. These results suggest that more than simple total error reduction determines responding after extinction.     

Conditioning of simultaneous and serial feature-positive discriminations

Three experiments with rat subjects examined the development of simultaneous and serial feature-positive discriminations in appetitive conditioning. In Experiment 1, reinforced presentations of a simultaneous light-tone compound were intermixed with nonreinforced presentations of either the light or the tone. The compound stimulus acquired conditioned behaviors of a form characteristic of the predictive feature alone; the element common to reinforced and nonreinforced trials did not evoke conditioned behavior. In Experiment 2, reinforced presentations of a serial light-trace-tone compound were intermixed with nonreinforced tone-alone presentations. The light feature stimulus acquired conditioned behaviors characteristic of visual CSs. The tone stimulus, common to reinforced and nonreinforced trials, evoked conditioned behaviors characteristic of auditory CSs, but only when preceded by the light. In Experiment 3, variations in the interval between the light and tone on reinforced trials had little effect on responding to the light CS but substantially altered the pattern of responding to the tone CS. These results suggested that simultaneous and serial feature-positive discriminations may be solved differently. Performance in simultaneous feature-positive discriminations may be determined solely by associations between the feature stimulus and the reinforcer, but performance in serial discriminations may also involve the acquisition of a conditional cue function to the feature.     

Associative properties of a conditioned inhibitor as a function of age in kittens

The efficacy of conditioned inhibition in a novel conditioned stimulus/conditioned inhibitor (CS/CI) compound was tested in 6-, 10-, and 14-week-old kittens. The conditioned response was suppression of respiration elicited by a 5.1-sec CS paired with a brief, mild footshock. During original inhibitory training, a CI was presented 2 sec after the onset of the CS, and the stimuli coterminated 3 sec later without the shock. As previously reported, the CI trained in this paradigm is more potent in older kittens but passes a summation test in all age groups (Dess & Soltysik, 1989). In the transfer test, the order of the CS and CI was reversed, so that the CI preceded the CS with no stimulus overlap. Transfer of inhibition to this new compound was virtually absent in the 6-week-old kittens and nearly perfect in the 14-week-old kittens. The CI alone (before CS onset) elicited a strong fear response in the youngest kittens, moderate fear in the 10-week-old group, and very little fear in the oldest group. The transferability of inhibitory training to a different temporal configuration of the CS and CI is absent at 6 weeks of age and fully developed 8 weeks later.     

Protection from extinction provided by a conditioned inhibitor

Three conditioned suppression experiments with rats as subjects investigated the influence of higher order associations in determining the response potential of a target stimulus. In these experiments, a Pavlovian conditioned inhibitor was compounded with the target cue during extinction treatment. In Experiment 1, strong suppression was observed to the target cue that was given extinction treatment in the presence of a conditioned inhibitor, relative to a target that was extinguished with an associatively neutral cue or was extinguished alone, suggestive of enhanced protection from extinction provided by a conditioned inhibitor. This effect was replicated in a sensory preconditioning preparation in Experiment 2; in Experiment 3, in a sensory preconditioning preparation, this protection effect was retroactively attenuated when the conditioned excitor used to train the conditioned inhibitor was extinguished following extinction of the target. This provides evidence that, at least in a sensory preconditioning preparation, stimuli that are only indirectly associated with the target cue can contribute to the response potential of that target.     

Positive and negative transfer of conditioned aversive stimuli to a conditioned appetitive excitor as a function of aversive US intensity

Rats were given Pavlovian aversive (Av) conditioning in which a weak (0.5-sec, 0.7-mA) or a strong (0.5-sec, 1.4-mA) footshock unconditioned stimulus (US) was presented alone or in a positive, zero, or negative correlation with a flashing-light conditioned stimulus (AvCS+, AvCSo, or AvCS?, respectively). Thereafter, the subjects received Pavlovian appetitive (Ap) conditioning in which the flashing-light CS was positively correlated in a forward order with the delivery of a food US. As anticipated, for subjects that had been trained with the strong shock US, the AvCS+ retarded and the AvCS? facilitated Ap conditioning relative to both the AvCSo and the novel-CS treatments, which did not differ in effect. However, the exact opposite prevailed for the AvCS+ and AvCS? subjects that had been trained with the weak shock US. On the basis of these and other data, we propose an “ABC” model of transfer that stresses the importance of affective, behavioral, and cognitive factors in accounting for the divergent results that are obtained in both Av-to-Ap and Ap-to-Av transfer paradigms.     

Two components of responding in Pavlovian lick suppression

The present research examined the temporal distribution of responding in a lick suppression paradigm. In Experiment 1, rats were trained with either a 30- or a 120-s conditioned stimulus (CS), which was followed either by a footshock (unconditioned stimulus [US]) or nothing. Licking during the CS was suppressed only in the former condition. Suppression was more pronounced early in the CS. In Experiment 2, rats were exposed to two 30-s or two 120-s CSs, with delivery of the shock being contingent on CS1 for half of the animals and on CS2 for the other half. For both the paired and the unpaired conditions, suppression at the beginning of CS1 was observed for all the groups. By discounting the possibility of generalization between CS1 and CS2, it appears that this initial suppression was not a conditioned response to the CS, but an unconditioned one due to mere exposure to the shock US.     

Nonassociative habituation,US preexposure,and backward inhibitory conditioning with signaled and unsignaled USs

In a conditioned suppression experiment, rats received a single, massed session of conditioning in which one backward conditioned inhibitory stimulus (CS-) followed shocks that were signaled by a visual cue, and a second backward CS-followed shocks that were unsignaled. Conditioning was preceded by a preexposure phase in which some groups of rats were preexposed to unsignaled shock, while others were not preexposed and remained in the experimental apparatus in the absence of shock. The groups were further distinguished by whether US preexposure and conditioning occurred in the same or different contexts, and by whether conditioning began immediately or after a 24-h rest period in the home cage. Although the conditioning itself was effective in establishing the visual cue as a conditioned excitor in the nonpreexposed groups, it was not effective in establishing the two backward cues as reliable inhibitors with either signaled or unsignaled USs. After 210 US preexposures, however, the same conditioning sessions did yield conditioned inhibition to both CS-s. A 24-h rest period in the home cage reduced the magnitude of, but did not completely abolish, the facilitative effect of US preexposure on inhibitory conditioning. Other tests demonstrated that US preexposure had retarded excitatory conditioning to the visual cue. This interference with excitatory conditioning was unchanged in magnitude after the 24-h rest period. The facilitative effect of US preexposure on backward inhibitory conditioning, and the interference effect on excitatory conditioning, were both eliminated by a change in context between US preexposure and conditioning. These observations encourage predominantly associative accounts of the effects, but allow for a small nonassociative habituation component.     

Signaling and affective functions in Pavlovian conditioning

The present study employed a Pavlovian-instrumental-transfer paradigm to investigate the role of conditioned fear in appetitive discrimination learning. Each of three Pavlovian training procedures was used to establish a conditioned fear excitor (CS+), a “neutral” CS (CSo), and a conditioned fear inhibitor (CS?). Then, the CSs were administered to rats in the three groups contingent upon the rewarded response in a difficult visual discrimination. In addition, half of each group received shock punishment for each incorrect response. Relative to CSo, CS+ facilitated performance in contrast to the usual interfering effect of conditioned suppressors; conversely, CS? retarded performance even when its reinforcing action (fear inhibition) was potentiated by punishment for the incorrect response. These results, together with other findings showing a reversed outcome when the CSs are administered for the incorrect response, indicate that Pavlovian conditioning comprises both general signaling and affective functions, the former reflecting a basic “expectancy” or nominal type of cognitive processing in the rat.     

Dissociation of conditioned appetitive and consummatory sexual behavior: Satiation and extinction tests

Sexual responses were conditioned in male Japanese quail using the opportunity to copulate with a female as the unconditioned stimulus (US). The conditioned stimulus (CS) was a 3-D object made of a taxidermically prepared female quail head mounted on a terry-cloth body. Both appetitive conditioned responses (approach and proximity to the CS) and consummatory conditioned responses (mount and cloacal contact directed toward the CS) developed when 2-min presentations of the CS were followed immediately by the US, but not when the CS and US were separated by trace intervals of 10 or 20 min (Experiment 1). Postconditioning sexual satiation suppressed conditioned cloacal contact responses more than conditioned approach to the CS (Experiment 2), and “acute” extinction suppressed both conditioned mounting and conditioned cloacal contact responses more than conditioned approach to the CS (Experiment 3). These results demonstrate a functional dissociation between conditioned appetitive and consummatory responses and imply that the motivational and/or associative mechanisms underlying the two types of behavior are distinct.