The effects of context extinction on US signal value

Two experiments with rats examined the effects of context extinction on responding to the signal value of an unconditioned stimulus (US). In Experiment 1, US signal value was first trained when a single food pellet signaled the delivery of three additional pellets. After training, rats received either context extinction (CE) or home cage (HC) exposure before testing US signal value by single food pellet presentations. Results showed responding was significantly reduced in Group CE compared to Group HC. Experiment 2 replicated Experiment 1 and showed that exposure to a different context did not reduce responding to the signal value of a US. The results complement research by Kehoe et al. [Kehoe, E. J., Weidemann, G., & Dartnall, S. (2004). Apparatus exposure produces profound declines in conditioned nictitating-membrane responses to discrete conditioned stimuli by the rabbit (Oryctolagus cuniculus). Journal of Experimental Psychology: Animal Behavior Processes, 30, 259–270.] and have key implications for prominent theories of conditioning.     

Using pavlovian higher-order conditioning paradigms to investigate the neural substrates of emotional learning and memory

In first-order Pavlovian conditioning, learning is acquired by pairing a conditioned stimulus (CS) with an intrinsically motivating unconditioned stimulus (US; e.g., food or shock). In higher-order Pavlovian conditioning (sensory preconditioning and second-order conditioning), the CS is paired with a stimulus that has motivational value that is acquired rather than intrinsic. This review describes some of the ways higher-order conditioning paradigms can be used to elucidate substrates of learning and memory, primarily focusing on fear conditioning. First-order conditioning, second-order conditioning, and sensory preconditioning allow for the controlled demonstration of three distinct forms of memory, the neural substrates of which can thus be analyzed. Higher-order conditioning phenomena allow one to distinguish more precisely between processes involved in transmission of sensory or motor information and processes involved in the plasticity underlying learning. Finally, higher-order conditioning paradigms may also allow one to distinguish between processes involved in behavioral expression of memory retrieval versus processes involved in memory retrieval itself.     

Trace and delay eyeblink conditioning: contrasting phenomena of declarative and nondeclarative memory

We tested the proposal that trace and delay eyeblink conditioning are fundamentally different kinds of learning. Strings of one, two, three, or four trials with the conditioned stimulus (CS) alone and strings of one, two, three, or four trials with paired presentations of both the CS and the unconditioned stimulus (US) occurred in such a way that the probability of a US was independent of string length. Before each trial, participants predicted the likelihood of the US on the next trial. During both delay ( n =20) and trace ( n = 18) conditioning, participants exhibited high expectation of the US following strings of CS-alone trials and low expectation of the US following strings of CS-US trials a phenomenon known as the gambler's fallacy. During delay conditioning, conditioned responses (CRs) were not influenced by expectancy but by the associative strength of the CS and US. Thus, CR probability was high following a string of CS-US trials and low following a string of CS-alone trials. The results for trace conditioning were opposite. CR probability was high when expectancy of the US was high and low when expectancy of the US was low. The results show that trace and delay eyeblink conditioning are fundamentally different phenomena. We consider how the findings can be understood in terms of the declarative and nondeclarative memory systems that support eyeblink classical conditioning.     

The Effects of a Pretrained Excitatory Stimulus on Schedule-Induced Polydipsia in the Rat

The purpose of the present study was to test two predictions derived from the application of Pavlovian conditioning principles to the schedule-induced polydipsia (SIP) phenomena. The first prediction was that a pretrained excitatory signal for pellet delivery would facilitate the development of SIP. A second prediction was that phenomena which are typically observed in Pavlovian conditioning experiments, such as learned irrelevance, latent inhibition, and the US preexposure effect, would also be observed in the SIP paradigm. The results indicated that a group given excitatory pretraining to a tone failed to develop SIP more rapidly than controls when this tone was used to signal pellet deliveries during SIP training. However, learned irrelevance, latent inhibition, and the US preexposure effect were demonstrated. Thus, these data generally support the predictions derived from the Pavlovian conditioning view of SIP.

     

Context modulation of US signal value

Context modulation of unconditioned stimulus (US) signal value was examined in two experiments. In Experiment 1, rats showed significantly more magazine entries after a single food pellet US in Context A (in which three additional pellets shortly followed) than in Context B (in which the delivery of three additional pellets was delayed). Experiment 2 replicated this effect and showed that any differences in contextual associative strength at the time the single food pellet was delivered did not importantly contribute to context modulation. Implications for theories of occasion setting and context modulation are considered.     

Bayesian theories of conditioning in a changing world

The recent flowering of Bayesian approaches invites the re-examination of classic issues in behavior, even in areas as venerable as Pavlovian conditioning. A statistical account can offer a new, principled interpretation of behavior, and previous experiments and theories can inform many unexplored aspects of the Bayesian enterprise. Here we consider one such issue: the finding that surprising events provoke animals to learn faster. We suggest that, in a statistical account of conditioning, surprise signals change and therefore uncertainty and the need for new learning. We discuss inference in a world that changes and show how experimental results involving surprise can be interpreted from this perspective, and also how, thus understood, these phenomena help constrain statistical theories of animal and human learning.     

The US-preexposure effect in lithium-induced flavor-aversion conditioning is a consequence of blocking by injection cues

In 2 experiments, rats received flavor-aversion conditioning in which the unconditioned stimulus (US) was an orally consumed solution of lithium chloride (LiCl). The resulting aversion was not attenuated by giving preexposure to injections of LiCl, although such preexposure did attenuate aversions established using injected LiCl as the US (Experiment 1). This outcome suggests that blocking by injection-related cues is responsible for the US-preexposure effect observed in this situation. Experiment 2 confirmed this interpretation by showing that presenting such cues (by giving an injection of saline) at the time that the LiCl was drunk resulted in an attenuation of conditioning in animals preexposed to injections of LiCl. The US-preexposure effect obtained in these experiments can be explained solely in terms of blocking by injection cues, although other mechanisms may contribute to the effect seen in other flavor-aversion paradigms.     

Effects of Early Hippocampal Lesions on Trace, Delay, and Long-Delay Eyeblink Conditioning in Developing Rats

The effects of bilateral hippocampal aspiration lesions on later acquisition of eyeblink conditioning were examined in developing Long-Evans rat pups. Lesions on postnatal day (PND) 10 were followed by evaluation of trace eyeblink conditioning (Experiment 1) and delay eyeblink conditioning (Experiment 2) on PND 25. Pairings of a tone conditioned stimulus (CS) and periocular shock unconditioned stimulus (US, 100 ms) were presented in one of three conditioning paradigms: trace (380 ms CS, 500 ms trace interval, 880 ms interstimulus interval [ISI]), standard delay (380 ms CS, 280 ms ISI), or long delay (980 ms CS, 880 ms ISI). The results of two experiments indicated that hippocampal lesions impaired trace eyeblink conditioning more than either type of delay conditioning. In light of our previous work on the ontogeny of trace, delay, and long-delay eyeblink conditioning (Ivkovich, Paczkowski, & Stanton, 2000) showing that trace and long-delay eyeblink conditioning had similar ontogenetic profiles, the current data suggest that during ontogeny hippocampal maturation may be more important for the short-term memory component than for the long-ISI component of trace eyeblink conditioning. The late development of conditioning over long ISIs may depend on a separate process such as protracted development of cerebellar cortex.     

Expectancy-learning and evaluative learning in human classical conditioning: affective priming as an indirect and unobtrusive measure of conditioned stimulus valence

It has been argued that in classical conditioning two processes might be operative. First, one may learn that the conditioned stimulus (CS+) is a valid predictor for the occurrence of the biologically negative or positive event (US; expectancy-learning). Second, one may learn to perceive the conditioned stimulus itself as a negative or positive stimulus, depending on the valence of the event it has been associated with (evaluative learning). Until the present, however, both forms of learning have been investigated using rather different conditioning procedures. Using a differential aversive conditioning preparation with pictures of human faces as CSs and an electrocutaneous stimulus as US, we were able to demonstrate that both forms of learning can co-occur. Moreover, the extent of evaluative learning in this aversive conditioning procedure did not significantly differ from the amount of evaluative learning in an evaluative conditioning procedure with positive and negative adjectives as USs, which was administered to the same participants. In the present study evaluative learning was not only indexed by direct evaluative ratings, but we introduced affective priming as an indirect and unobtrusive, reaction time based measure of stimulus valence. Finally, imagery instructions during acquisition did not facilitate expectancy-learning nor evaluative learning.     

Context blocking in rat autoshaping: Sign-tracking versus goal-tracking

Prior experience of unsignaled food can interfere with subsequent acquisition by birds of autoshaped key-pecking at a signal light. This has been understood to indicate that unsignaled food results in context conditioning, which blocks subsequent learning about the keylight-food relationship. In the present experiment with rats lever insertion as the conditioned stimulus (CS) preceded sucrose delivery as the unconditioned stimulus (US). Half the rats initially received unsignaled USs in the conditioning context, while the remainder did not. Both lever-presses (sign-tracking) and magazine-entries (goal-tracking) were recorded. Under immediate reinforcement conditions, prior unsignaled US interfered with sign-tracking, but had no effect on goal-tracking. In two further groups, a trace condition prevented development of sign-tracking. In this case, prior context conditioning interfered with goal-tracking. These results suggest that interference with sign-tracking may reflect response competition, while interference with goal-tracking under trace conditions may reflect failure to acquire a CS-US association.     

Pavlovian conditioning: the CS-UR relation

A new Pavlovian procedure used fluid-elicited throat-movement responses of the pigeon (N=66) to study the effects on conditioning of the temporal relation of the conditioned stimulus (CS) to the unconditioned stimulus-unconditioned response (US-UR). Because the throat-movement response has a substantial latency and duration, the relation of the CS to the US and UR could be independently evaluated. Four experiments indicated that, operationally, the relation of the CS to the UR--not to the US--is critical for conditioning in this preparation. The conventional emphasis on CS-US relations is based on procedures that confound the occurrence of the US with the UR and that foster generalization decrement between training and testing. The authors indicate how several conditioning phenomena may be reinterpreted in terms of CS-UR relations.     

Aversive conditioning under conditions of restricted awareness: Effects on spatial cueing

In the literature on aversive conditioning there is still debate on the role of awareness. According to some authors, affective learning can occur with or without contingency learning (dual-process model), whereas others argue that a single process produces both affective responses and contingency knowledge. Although many studies have investigated these models, the results to date are inconclusive. Based on a review of the literature, a new series of experiments was designed to examine aversive conditioning in the absence of contingency awareness. In the present study we examined the effects of subliminal aversive conditioning on a spatial cueing task. Awareness was stringently tested after conditioning. Three kinds of awareness were distinguished: contingency awareness (awareness of the CS?US contingencies, where CS is the conditioned stimulus, and US is the unconditioned stimulus), perceptual awareness (awareness of the perceptual differences between the CSs), and US expectancy (awareness of a threat feeling when confronted with the CS+, but not when confronted with the CS?). The results of three experiments demonstrated that responses on the spatial cueing task were modulated by subliminal aversive conditioning. Importantly, none of the participants was contingency aware or able to perceptually discriminate between the conditioned stimuli. However, in Experiment 3, only those participants showing some level of postconditioning expectancy awareness exhibited conditioning effects. These experiments suggest that subliminal aversive conditioning produces small but significant effects, which may be modulated by expectancy awareness.     

Latent inhibition of US signal value.

Three experiments with rats examined the effects of preexposure to an unconditioned stimulus (US; a single food pellet) on the subsequent ability of that US to effectively signal the delivery of three food pellets during a US-US conditioning procedure. In Experiment 1, latent inhibition (LI) rats showed attenuated conditioning, compared to control (C) rats, when a single food pellet, delivered 10 minutes into a session, was followed by three additional pellets. In preexposure, one pellet had been delivered 10 minutes into each session (in group LI), or placed into the magazine at the beginning of each session (in group C). Experiment 2 showed that this effect was evident when the conditions of preexposure matched those of conditioning for group C, and Experiment 3 showed that the difference between groups LI and C was not a product of context conditioning, or latent inhibition to the noise of the feeder in group LI. Implications of these results for theories of latent inhibition are considered.     

Mechanisms underlying retarded emergence of conditioned responding following inhibitory training: evidence for the comparator hypothesis

The comparator hypothesis posits that conditioned responding is determined by a comparison at the time of testing between the associative strengths of the conditioned stimulus (CS) and stimuli proximal to the CS at the time of conditioning. The hypothesis treats all associations as being excitatory and treats conditioned inhibition as the behavioral consequence of a CS that is less excitatory than its comparator stimuli. Conditioned lick suppression by rats was used to differentiate four possible sources of retarded responding to an inhibitory CS. These include habituation to the unconditioned stimulus (US), latent inhibition to the CS, blocking of the CS-US association by the conditioning context, and enhanced excitatory associations to the comparator stimuli. Prior research has demonstrated the first three phenomena. Therefore, we employed parameters expected to highlight the fourth one--the comparator process. In Experiment 1, our negative contingency training was shown to produce a conditioned inhibitor that passed inhibitory summation and retardation tests. In Experiment 2 we found transfer of retardation from an inhibitory CS to a novel stimulus when the location where retardation-test training occurred was excitatory, which is indicative of contextual blocking and/or comparator effects. In Experiment 3, extinction of the conditioning context was found to attenuate retardation regardless of whether extinction occurred before or after the CS-US pairings of the retardation test. This indicates that much of the present retardation was due to the comparator process rather than to contextual blocking. Experiment 4 demonstrated that habituation to the US did not contribute to retardation in the present case. Collectively, these studies suggest that retardation following inhibitory training can be explained without recourse to any of the traditional mechanisms of conditioned inhibition.     

Taste aversions conditioned by the aversiveness of insulin and formalin: role of CS specificity

Experimenters in the past have reported that when insulin is used as the unconditioned stimulus (US), rats will learn an aversion to a sodium chloride but not a sucrose solution, whereas with formalin as the US, they will learn an aversion to a sucrose but not a saline solution. The present experiments failed to confirm these findings. Aversions to sucrose were conditioned with insulin and aversions to sodium chloride were conditioned with formalin. The use of a more concentrated sucrose solution in the present study may have been responsible for the successful sucrose-aversion conditioning with insulin. Although the source of the discrepancy in findings concerning aversion conditioning with formalin remains unclear, experiments ruled out numerous possibilities. These experiments also showed that sodium chloride aversion conditioning with formalin is a highly robust phenomenon that occurs with a variety of conditioned stimulus durations and formalin doses, with distributed and massed training, in male and female rats, and even if saline is not the only novel solution presented during conditioning. Furthermore, the aversion can be detected with both single-stimulus and choice test procedures.     

Integrating incremental learning and episodic memory models of the hippocampal region

By integrating previous computational models of corticohippocampal function, the authors develop and test a unified theory of the neural substrates of familiarity, recollection, and classical conditioning. This approach integrates models from 2 traditions of hippocampal modeling, those of episodic memory and incremental learning, by drawing on an earlier mathematical model of conditioning, SOP (A. Wagner, 1981). The model describes how a familiarity signal may arise from parahippocampal cortices, giving a novel explanation for the finding that the neural response to a stimulus in these regions decreases with increasing stimulus familiarity. Recollection is ascribed to the hippocampus proper. It is shown how the properties of episodic representations in the neocortex, parahippocampal gyrus, and hippocampus proper may explain phenomena in classical conditioning. The model reproduces the effects of hippocampal, septal, and broad hippocampal region lesions on contextual modulation of classical conditioning, blocking, learned irrelevance, and latent inhibition.     

Learned Irrelevance Is Not the Sum of Exposure to CS and US

In three experiments hungry rats received appetitive conditioning trials with a light that signalled the delivery of sucrose solution. In Experiment 1, prior exposure to uncorrelated presentations of the conditioned stimulus (CS) and unconditioned stimulus (US) retarded conditioning significantly more than did prior exposure to the CS alone. In Experiments 2 and 3, groups exposed to uncorrelated presentations of the CS and US within the same session conditioned significantly more slowly than groups given separate sessions of exposure to the CS followed by sessions of exposure to the US (or vice versa). Some part of the learned irrelevance effect depends on exposure to a zero correlation between the CS and US, perhaps because this promotes learning that the CS predicts no change in the probability of the US.     

A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning

Convergent data suggest dissociated roles for the lateral (LA) and basolateral (BLA) amygdaloid nuclei in fear conditioning, depending on whether a discrete conditioned stimulus (CS)-unconditional stimulus (US) or context-US association is considered. Here, we show that pretraining inactivation of the BLA selectively impaired conditioning to context. In contrast, inactivation of the LA disrupted conditioning to the discrete tone CS, but also either impaired or enhanced contextual conditioning, depending on whether the context was in the foreground or in the background. Hence, these findings refine the current model of the amygdala function in emotional learning by showing that the BLA and the LA not only differentially contribute to elemental and context-US association, but also promote, through their interaction, the most relevant of these two associations.     

Galantamine facilitates acquisition of a trace-conditioned eyeblink response in healthy, young rabbits

Previous work has demonstrated that drugs increasing brain concentrations of acetylcholine can enhance cognition in aging and brain-damaged organisms. The present study assessed whether galantamine (GAL), an allosteric modulator of nicotinic cholinergic receptors and weak acetylcholinesterase inhibitor, could improve acquisition and retention of an eyeblink (EB) classical conditioning task in healthy, young animals. We trained 24 rabbits (n = 8/group) in a 1000-msec trace Pavlovian EB conditioning paradigm in which a tone conditioned stimulus (CS) was presented for 500 msec, followed by a 500-msec trace period in which no stimuli were presented. A 100-msec corneal airpuff was the unconditioned stimulus (US). Acquisition sessions, consisting of 100 trials each, occurred daily for 10 consecutive days, followed by 3 d of extinction training. Animals were treated with one of three doses of GAL (0.0-3.0 mg/kg) prior to each session. Animals that received 3.0 mg/kg GAL showed significantly more EB conditioned responses (CRs) in fewer training trials than animals receiving either 1.5 mg/kg GAL or vehicle injections. GAL had no effect on CR performance during extinction. Pseudoconditioning control experiments, consisting of 200 explicitly unpaired tone-puff presentations indicated that GAL did not increase reactivity to the CS or US. These findings indicate that GAL may improve acquisition of moderately difficult associative learning tasks in healthy young organisms.     

Behavior systems,associationism, and Pavlovian conditioning

Associative and behavior systems accounts of Pavlovian conditioning have different emphases. The traditional associative account has focused on the role of the unconditional stimulus (US) in strengthening stimulus associations according to a set of general laws. The behavior systems account has focused on the relation of conditional responding to the preorganized perceptual, motor, and motivational organization engaged by the US. Knowledge of a behavior system enables successful prediction of the form and ease of conditioning as a function of the type of conditional stimulus (CS), US, and the CS-US relation. At the same time, Pavlovian manipulations act as a window on how a behavior system works. Both associative and behavior systems accounts can be criticized as incomplete and idiosyncratic. A comprehensive account of Pavlovian conditioning could profit from their integration.