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.     

Context effects on conditioning,extinction, and reinstatement in an appetitive conditioning preparation

Three experiments with rat subjects examined the effects of contextual stimuli on performance in appetitive conditioning. A 10-sec tone conditioned stimulus (CS) was paired with a food-pellet unconditioned stimulus (US); conditioning was indexed by the observation of headjerking, a response of the rat to auditory stimuli associated with food. In Experiment 1, a context switch following initial conditioning did not affect conditioned responding to the tone; however, when the response was extinguished in the different context, a return to the original conditioning context “renewed” extinguished responding. These results were replicated in Experiments 2 and 3 after equating exposure to the two contexts (Experiment 2) and massing the conditioning and extinction trials (Experiment 3). The results of Experiment 1 also demonstrated that separate exposure to the US following extinction reinstates extinguished responding to the tone; this effect was further shown to depend at least partly on presenting the US in the context in which testing is to occur (Experiments 2 and 3). Overall, the results are consistent with previous data from aversive conditioning procedures. In either appetitive or aversive conditioning, the context may be especially important in affecting performance after extinction.     

Conditioned suppression is an inverted-U function of footshock intensity

Most theories of associative learning assert that conditioned responding to a target cue is a monotonically increasing function of unconditioned-stimulus (US) intensity. In a lick suppression preparation with rats, a cue was paired with a 0.4-, 0.6-, 0.8-, 1.0-, 1.2-, or 1.4-mA footshock in Experiment 1a, and with a 0.3-, 0.8-, 1.3-, or 1.8-mA footshock in Experiment 1b. Subsequent suppression in response to the cue was an inverted-U function of the US intensity. In Experiment 2, we demonstrated that massive extinction of the training context and compound conditioning can each attenuate the response decrement caused by training with a high-intensity US. The sometimes-competing-retrieval model (Stout & Miller, Psychological Review 114:759–783, 2007) provides a better fit to these data than do several other models of associative learning.     

Chemosensory-based contextual conditioning inHermissenda crassicornis

In two experiments, the marine molluskHermissenda crassicornis was exposed to context discrimination training. In one context, defined by the presence of a diffuse chemosensory stimulus (shellfish extract A), brief, unsignaled, unconditioned stimuli (USs; high-speed rotation) were presented; in a second context, defined by the presence of shellfish extract B, no USs were presented. Animals were then tested (at both 1.5 and 24 h) by exposing them to small pieces of the shellfish meat used to define the two contexts. The latency to strike at the meat served as an index of the context-US association. In Experiment 1, the latency to strike at the cue associated with rotation was reduced relative to both preconditioning strike latencies and the associatively neutral cue. However, in a two-choice test where the animals could approach the conditioned or neutral stimulus, the animals regularly avoided the stimulus paired with rotation. Moreover, if, following conditioning, the animals were presented with an unsignaled rotation in the conditioned context or the neutral context, the animals exhibited more effective defensive clinging (an unconditioned reflex normally elicited by rotation) in the conditioned context, suggesting that it “prepared” the animal for the aversive US. In total, these results demonstrate thatHermissenda is capable of making associations to diffuse background (contextual) stimuli. Moreover, the results suggest that pairing the chemosensory cue with an aversive US elicits a strike response inHermissenda when the animal is placed in forced contact with the cue and an active avoidance response when the animal can choose between that cue and a neutral cue.     

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.     

Independent effects of stimulus and cycle duration in conditioning: The role of timing processes

Rats received delay conditioning procedures with a white-noise conditioned stimulus (CS), a food unconditioned stimulus (US), and head entries into the food cup as the conditioned response. The stimulus duration (S) and the interval between food deliveries (C) were varied between groups:S=15, 30, 60, and 120 sec;C=90, 180, and 360 sec. The stimulus/cycle duration ratio was negatively related to the asymptotic level of conditioning but had no effect on the rate of acquisition. Conditioning and timing of responses emerged together in training. Timing occurred during the CS-US interval (ISI) and the US-US interval (ITI), as evidenced by increasing response rate gradients that were steeper for shorter intervals. The effects of the stimulus/cycle ratio on conditioning were attributed to independent timing of theS andC durations. Serial-, parallel-, and single-process accounts of conditioning and timing are compared.     

Conditioned avoidance responses survive contingency degradation in the garden slug,Lehmannia valentiana

Joint presentations of a conditioned stimulus (CS) and an unconditioned stimulus (US) strengthen the contingency between them, whereas presentations of one stimulus without the other degrade this contingency. For example, the CS can be presented without the US either before conditioning (CS–no US and then CS–US; latent inhibition) or after conditioning (CS–US and then CS–no US; extinction). In vertebrate subjects and several invertebrate species, a time lapse usually results in a return of the conditioned response, or spontaneous recovery. However, in land mollusks, spontaneous recovery from extinction has only recently been reported, and response recovery after latent inhibition has not been reported. In two experiments, using conditioned aversion to a food odor as a measure of learning and memory retention, we observed contingency degradation via latent inhibition (Experiment 1) and extinction (Experiment 2) in the common garden slug, Lehmannia valentiana. In both situations, the contingency degradation procedure successfully attenuated conditioned responding, and delaying testing by several days resulted in recovery of the conditioned response. This suggests that the CS–US association survived the degradation manipulation and was retained over an interval of several days.     

Stimulus competition in the absence of compound conditioning

Most associative theories have assumed that stimulus competition occurs only between conditioned stimuli (CSs) that are trained in compound. The present research investigated the possibility of competition between two CSs that were individually paired to the same unconditioned stimulus (US). We used human subjects in an anticipatory suppression analogue to Pavlovian conditioning. Experiment 1 showed that X+ training followed by A+ training resulted in impaired responding to X. This did not occur when A+ training preceded X+ training. Experiment 2 replicated the basic effect and showed that it did not occur when the Phase 2 training consisted of A? instead of A+ nor when the A+ pairings occurred in a second context. Experiment 3 showed that A+ pairings occurring in a second context could still produce the effect when X was tested in the context in which the A+ pairings had occurred, but not when X was tested in a context different from that used for A+ training. Collectively, these results suggest that individually trained CSs may compete with each other when one of those CSs is more strongly activated by the test context than the other one.     

Differential second-order aversive conditioning using contextual stimuli

Two experiments were conducted to determine if contextual stimuli used as S₂ in a higher-order differential conditioning procedure would control the performance of rats. Discrete stimuli were first paired with footshock in a separate training context. During second-order training, a shock-associated discrete stimulus was presented in one of two discriminable observation chambers. Over 4 days of training, subjects engaged in more freezing in the context associated with an excitatory discrete S₁, relative to a context in which no discrete stimulus, or a stimulus that had been explicitly unpaired with shock delivery, was presented. After acquisition of the second-order discrimination, animals were returned to the original training context where they received a “signaled inflation” treatment designed to change the current value of S₁, and the US. This postconditioning manipulation did not selectively affect performance of defensive freezing or conditional analgesia in S₂.     

Dominance,the bidirectional hypothesis,and Pavlovian backward conditioning in the US-US paradigm

Based upon considerations raised by Soviet research, the role of relative stimulus intensity, or dominance, in the unconditioned stimulus-unconditioned stimulus (US-US) paradigm was investigated under circumstances presumed favorable to the backward conditioned response (CR). Using the classically conditioned forelimb response of the cat, a brief shock (USD delivered to one forepaw preceded a shock (US2) to the opposite forepaw in paired conditioning fashion; subjects in the control group received explicitly unpaired presentations of the stimuli. Conditioning in both the forward and backward directions was evaluated by the appearance of contralateral CRs on test trials to each of the USs. In Experiment 1, a ratio of the intensities between US1 and US2 of 100:80 was used to create a relative dominance in favor of the backward CR. In addition, to evaluate the suggestion that the appearance of the backward CR is retarded in the Pavlovian paradigm, overtraining was provided to a forward conditioning criterion of 200%. In Experiment 2, the cats were exposed to successive reductions in the intensity of US2 to verify manipulations of dominance reportedly involved in the reactivation of a latent backward CR. Although forward conditioning was readily established to USl, there was no evidence of back-ward conditioning to US2 under any of the conditions.     

Pavlovian appetitive conditioning under curare in rats

A CS was paired with rewarding intracranial stimulation while Ss were immobilized by curare. Tests of the activity response to the CS were carried out before and after conditioning. With either simple or discriminative conditioning, activity to the rewarded CS increased after training. These results are comparable to those in studies using food reward and support the hypothesis that a central motivational state is conditioned to stimuli preceding reward.     

Stimulus preexposure speeds or slows subsequent acquisition of associative learning depending on learning test procedures and response measure

Prior exposure to a conditioned stimulus (CS) typically results in latent inhibition—slower acquisition of associative learning about that stimulus in subsequent training. Here, we found that CS preexposure had different effects on the appetitive conditioning of rats with a sucrose unconditioned stimulus (US) depending on training test procedures, the similarity of preexposure and training procedures, and the choice of response measure. Preexposure to a visual or an auditory stimulus produced facilitation of acquisition of food-cup-directed responding when both of those cues were (separately) paired with sucrose delivery in the training test (Experiments 1 and 3). By contrast, the same preexposure procedure resulted in latent inhibition of food-cup learning if the second stimulus in the test phase was of the same modality as the preexposed stimulus (Experiment 2). In Experiment 3, latent inhibition was enhanced if both phases included a single CS or both phases included both auditory and visual CSs, compared to treatments in which only one CS was presented in one phase but two CSs were presented in the other phase. In Experiment 4, preexposure of an auditory cue slowed subsequent learning about it if the context was salient but enhanced learning if the context was of weaker salience. Finally, a measure of general activity revealed latent inhibition after preexposure in all conditions in all 4 experiments. We discuss the results within several classes of latent inhibition theories, none of which provides a comprehensive account.     

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.     

Conditioned cardiac and behavioral response topography to an olfactory CS dissociates with age

Conditioned cardiac and behavioral responses to an olfactory stimulus (CS) paired with electric shock (US) were studied in 16-, 23-, and 75-day-old rats. Heart rate and behavior were recorded during a single 15-trial training session in which a 10-sec olfactory stimulus (amyl acetate) was either paired or explicitly unpaired with the US. In the preweanling rats, the conditioned cardiac response consisted of anincrease in heart rate (tachycardia) and a slight increase in investigatory behaviors. In contrast, the conditioned cardiac response in the adult rats consisted of adecrease in heart rate (bradycardia) and a striking increase in behavioral immobility (freezing). The 23-day-old rats showed a dichotomous pattern of responding; some showed preweanling-like conditioned responses and some showed adultlike responses. Developmental changes in neural organization and degree of learning are discussed as possible determinants of the transition from infant to adult modes of responding.     

Renewal of Pavlovian conditioned inhibition

Prior research has demonstrated renewal, which is the ability of contextual cues to modulate excitatory responding to a Pavlovian conditioned stimulus (CS). In the present research, conditioned lick suppression in rats was used to examine similar contextual modulation of Pavlovian conditioned inhibition. After Pavlovian conditioned inhibition training with a CS in one context, subjects were exposed to pairings of the CS with an unconditioned stimulus (US) either in the same or in a second context. Results indicated that, when the CS was paired with the US in the second context, the CS retained its inhibitory control over behavior, provided that testing occurred in the context used for inhibition training. However, when the CS-US pairings occurred in the inhibition training context, the CS subsequently proved to be excitatory regardless of where testing occurred. These observations indicate that conditioned inhibition is subject to renewal.     

Cross-modal transfer as a function of initial training level in classical conditioning with the rabbit

Initial reinforced training with a conditioned stimulus (CSA) from one sensory modality subsequently facilitates the rate of acquisition of the rabbit’s nictitating membrane response to a second conditioned stimulus (CSB) from a different sensory modality. In Experiment 1, the level of transfer was a direct function of the number of CSA-US pairings (0, 15, 30, 60, and 120). In Experiment 2, cross-modal transfer appeared to be maximal after initial training was conducted to a performance criterion as small as two CRs to CSA. The results are discussed with respect to theories of transfer, particularly a layered network model of conditioning that suggests that CR acquisition to each CS depends on two sequentially organized associations, one unique to the CS and one that is common to all associations involving the target response system.     

Effects of US parameters on classical conditioning of cat hindlimb flexion

Unconditioned stimulus (US) intensity and duration were manipulated to determine their effects on cat hindlimb flexion conditioning. Seven consecutive days of acquisition training of a hindlimb flexor response to a tone conditioned stimulus (CS) were followed by 2 days of extinction. Eight animals in each of 12 groups received a 1-, 2-, 3-, or 4-mA, 60-Hz shock delivered to the right hindleg for 25, 50, or 100 msec as the US. Analysis of conditioned-response (CR) frequency indicated that conditioned responding was a positive function of both the intensity and duration of shock, although these variables did not interact with one another. CR latency and amplitude were decreased and increased, respectively, by increases in US intensity. The pattern of results reported here may support a contiguity notion of conditioning, and are discussed in the context of other conditioning preparations.     

Conditioning of tentacle lowering in the snail (Helix aspersa): Acquisition, latent inhibition, overshadowing, second-order conditioning, and sensory preconditioning

In a series of related experiments, we studied associative phenomena in snails (Helix aspersa), using the conditioning procedure of tentacle lowering. Experiments 1A and 1B demonstrated a basic conditioning effect in which the pairing of an odor (apple) as the conditioned stimulus (CS) with the opportunity to feed on carrot as the unconditioned stimulus (US) made snails exhibit increased levels of tentacle lowering in the presence of the CS. Experiments 2 and 3 showed that the magnitude of the conditioning was reduced when snails were exposed to the CS prior to the conditioning trial (a latent inhibition effect). Experiment 4 examined the effects produced by pairing a compound CS (apple—pear) with food presentations and demonstrated the existence of an overshadowing effect between the two odors. Experiment 5 revealed that pairing one CS with another previously conditioned stimulus increased tentacle lowering to the new CS (a second-order conditioning effect). Finally, Experiment 6 showed that pairing two odors prior to conditioning of one of them promoted an increase in tentacle lowering in response to the other (a sensory preconditioning effect). The results are discussed in terms of an associative analysis of conditioning and its implications for the study of cognition in invertebrates.     

Conditioned inhibition training of the competing cue after compound conditioning does not reduce cue competition

In each of two experiments, we studied Pavlovian fear conditioning (as assessed by barpress conditioned suppression) in 32 albino rats. Following a two-stage cue-competition procedure (A+ then AX+), we subjected the competing cue (A) to conditioned inhibition training (B+, BA?) before testing the target cue (X). Conditioned inhibition training was designed to weaken the putative A-unconditioned stimulus (US) association, perhaps changing it to an A-no-US association. Performance-deficit theories of cue competition, such as comparator theory and retrieval-interference theory, predict that such procedures should weaken cue competition, causing Conditioned Stimulus X (CS X) to evoke strong responding. The same prediction can be deduced from recent acquisition-focused models (Dickinson &; Burke, 1996; Van Hamme &; Wasserman, 1994). In opposition to this prediction, however, we found in both experiments that conditioned inhibition training had no detectable effect on cue competition even though it successfully abolished conditioned responding to CS A. In Experiment 2, moreover, we found evidence against the hypothesis that the weak response to CS X was due to generalization decrement rather than to cue competition. Results favor early learning-deficit theories of cue competition over performance-deficit theories and over the recent acquisition-focused models.     

Fear-potentiated startle using three conditioned stimulus modalities

The capacities of three different conditioned stimulus modalities (light, noise, and airflow produced by a fan) to produce fear-potentiated startle were evaluated. Previous experiments have shown that following either light-shock or noise-shock pairings, both the light and noise conditioned stimuli acquire the ability to potentiate the acoustically elicited startle response in rats (the so-calledfear-potentiated startle effect). In Experiment 1, the ability of airflow produced by a fan to act as a conditioned stimulus was investigated. Rats were given either paired or impaired fan-shock training followed by a test for fear-potentiated startle. The fan conditioned stimulus potentiated startle only in the group given explicit fan-shock pairings. In Experiment 2, we evaluated the discriminability of the three conditioned stimulus modalities. Rats were given light, noise, or fan-shock pairings and were subsequently tested for fear-potentiated startle with the trained conditioned stimulus as well as the two remaining novel conditioned stimuli. Only the trained conditioned stimulus potentiated startle. These results show that fear-potentiated startle can be produced with three discriminable conditioned stimulus modalities, allowing the future use of fear-potentiated startle in the investigation of higher order conditioning phenomena.