Revisiting the learning-without-awareness question in human pavlovian autonomic conditioning: Focus on extinction in a dichotic listening paradigm

Numerous studies have indicated that, consistent with current “cognitive” accounts of information processing, human Pavlovian autonomic discrimination acquisition cannot occur without awareness of the CS-US relationship. However, extinction studies have suggested that awareness is not necessary, findings that, in information-processing terms, have been explained by assuming that the processing by the extinction stage is parallel (automatic) rather than serial (controlled). This explanation was tested in an 80-subject study. The first, acquisition phase was a standard semantic differential conditioning arrangement with a 96-db white noise as US, and a “long” CS-US interval of 8 s, with ten trials each of CS+ (paired with US) and CS− (unpaired) trials. In extinction (USs omitted), in order to obtain non-autonomic indices of processing and thereby test the information-processing account of “unaware” autonomic conditioning during extinction, a dichotic listening task was implemented, with the CSs presented in the unattended channel (ear), while the subject had to perform a semantic differential reaction task in an attended-to channel (other ear). In early extinction, the electrodermal response occurring at an interval of 9–15 s after CS onset (i.e., following placement of the US during acquisition) and the finger-pulse-volume response occurring at an interval of 4–11 s after CS onset both showed reliable conditioning, but reaction-time and subjective-report data for the recognized critical words indicated serial rather than parallel processing of the CSs during extinction.     

Classical conditioning and information processing: Different mechanism for prepared and unprepared stimuli?

Although learning without awareness conflicts with recent theories of classical human Pavlovian conditioning, there is at least one type of conditioning in which CS-US contingency is processed without awareness—the so-called prepared conditioning. Therefore, presenting a secondary reaction time probe to measure the amount of information processing capacity required should produce interference with the secondary task in unprepared, but not in prepared conditioning, since in the latter information should be processed in parallel. In a previous study, the authors could not find differences between both types of conditioning, neither in reaction time nor in electrodermal indicators of information processing. The present study was conducted to replicate and extend these findings, using a differential autonomic conditioning paradigm. One half of 42 subjects received spider and snake slides as prepared stimuli, while the other half received flower slides as unprepared stimuli. Both kinds of stimuli were used as CS+ and as CS-. An electric shock served as unconditioned stimulus. During 24 acquisition and 24 extinction trials, electrodermal and heart rate responses, as well as reaction times to a probe stimulus, were recorded. The results revealed significant conditioning effects in terms of CS-/CS+ differences. However, no differences were found between prepared and unprepared stimuli, neither in autonomic measures nor in reaction time. Again, our results are in favor of serial information processing in both prepared and unprepared stimuli, suggesting that the so-called prepared conditioning may be treated as a subclass of classical autonomic conditioning instead of forming a specific class of learning.     

Electrodermal pavlovian conditioning with prepared and unprepared stimuli

One-trial learning referred to by Guthrie has been suggested to occur in autonomic conditioning, if the conditional stimuli (CSs) are so-called prepared ones. To test this idea, half of 28 subjects were given spider or snake slides as “prepared” CSs, while the remainder were given neutral slides as “unprepared” CSs. A shock was employed as the unconditional stimulus (UCS), with a CS-UCS interval of 8 seconds. Electrodermal activity and probe reaction times were the dependent measures of conditioning, conceived in cognitive, information-processing terms as the learning of the CS/UCS contingency. Evidence for the usual CS/UCS contingency learning emerged in both indicators, and during both acquisition and extinction, but none for one-trial learning, perhaps because the UCS was insufficiently aversive.     

Analyzing the random control procedure: Effects of paired and unpaired CSs and USs on autoshaping the chick's key peck with heat reinforcement

A series of five experiments using a total of 264 subjects investigated the effects of paired and unpaired key light (CS) and heat (US) stimuli on autoshaping the chick's key peck. Experiment 1 established that paired presentations of CS and US promoted a more rapid rise in key pecking than did randomly presented CSs and USs and that the specific sequence of stimuli under the random control procedure affected key pecking performance. Experiment 2 used a trace conditioning procedure to determine the role of the CS-US interval on autoshaping and to define empirically unpaired CSs and USs. Key pecking declined as the trace delay interval was increased from 0 to 25 sec; at 25 sec, no conditioning of key pecking occurred. Experiments 3–5 assessed the effects on autoshaped key pecking of (a) number of daily CS-US pairings, (b) added unpaired CS presentations, and (c) added unpaired US presentations, since paired and random control schedules differed in all of these respects. Reduction in the number of CS-US pairings slowed the acquisition of key pecking as did the concurrent addition of nonreinforced CSs and unsignaled USs. These results support theories of association formation that stress the effects of both paired and unpaired CSs and USs.     

The potentiation effect during serial conditioning

The development of suppression in rats to a target conditioned stimulus (CS) was compared in trace and serial conditioning procedures. The interval between the end of the target CS and the shock unconditioned stimulus (US) was filled by a second CS in the serial, but not the trace, procedure. In five experiments the serial procedure produced superior conditioning. This potentiation effect, however, depended critically upon the level of conditioning to the stimulus interpolated between the target CS and the US. When conditioning to the interpolated CS was either reduced by giving independent nonreinforced trials with this CS alone or enhanced by independent reinforced trials, the potentiation effect was abolished. In addition, the insertion of a trace interval between the target and interpolated CSs reduced the effect. However, the magnitude of conditioning to the target CS was unaffected by post-conditioning changes in the conditioned strength of the interpolated CS. These findings are discussed in terms of the contribution of both the association between the CSs themselves, which is inherent in the serial procedure, and that between the target CS and the US.     

Spontaneous recovery after extinction of the conditioned proboscis extension response in the honeybee

In honeybees, the proboscis extension response (PER) can be conditioned by associating an odor stimulus (CS) to a sucrose reward (US). Conditioned responses to the CS, which are acquired by most bees after a single CS-US pairing, disappear after repeated unrewarded presentations of the CS, a process called extinction. Extinction is usually thought to be based either on (1) the disruption of the stored CS-US association, or (2) the formation of an inhibitory "CS-no US" association that is better retrieved than the initial CS-US association. The observation of spontaneous recovery, i.e., the reappearance of responses to the CS after time passes following extinction, is traditionally interpreted as a proof for the formation of a transient inhibitory association. To provide a better understanding of extinction in honeybees, we examined whether time intervals during training and extinction or the number of conditioning and extinction trials have an effect on the occurrence of spontaneous recovery. We found that spontaneous recovery mostly occurs when conditioning and testing took place in a massed fashion (1-min intertrial intervals). Moreover, spontaneous recovery depended on the time elapsed since extinction, 1 h being an optimum. Increasing the number of conditioning trials improved the spontaneous recovery level, whereas increasing the number of extinction trials reduced it. Lastly, we show that after single-trial conditioning, spontaneous recovery appears only once after extinction. These elements suggest that in honeybees extinction of the PER actually reflects the impairment of the CS-US association, but that depending on training parameters different memory substrates are affected.     

Aware and (dis)liking: item-based analyses reveal that valence acquisition via evaluative conditioning emerges only when there is contingency awareness

Evaluative conditioning (EC) refers to changes in the liking of an affectively neutral stimulus (the conditioned stimulus, or CS) following the pairing of that stimulus with another stimulus of affective value (the unconditioned stimulus, or US). In 3 experiments, the authors assessed contingency awareness, that is, awareness of the CS-US associations, by relying on participants' responses to individual items rather than using a global method of assessment. They found that EC emerged on contingency aware CSs only. Of note, whether the CSs were evaluated explicitly (Experiments 1 and 2) or implicitly (Experiment 3) did not make a difference. This pattern supports the idea that awareness of the CS-US associations may be required for valence acquisition via EC.     

Evaluative conditioning in the picture-picture paradigm with random assignment of conditioned stimuli to unconditioned stimuli

Human participants were allocated to 1 of 3 groups. In the conditioning group, each conditioned stimulus (CS)-unconditioned stimulus (US) pair was presented 7 times during the acquisition phase. Participants who were assigned to the extinction group saw 5 additional presentations of each CS in isolation after the 7 presentations of each CS-US pair. In the latent inhibition group, the CS-only trials were presented before the CS-US trials. Overall, a significant evaluative conditioning effect was observed. This effect cannot be dismissed on the basis of the arguments developed by A. P. Field and G. C. L. Davey (1997, 1998, 1999), and the results thus provide strong evidence for the associative nature of evaluative conditioning. The results are also in line with other findings, which showed that evaluative conditioning is resistant to extinction.     

Learning with arbitrary versus ecological conditioned stimuli: Evidence from sexual conditioning

Laboratory investigations of Pavlovian conditioning typically involve the association of an arbitrary conditioned stimulus (CS) with an unconditioned stimulus (US) that has no inherent relation to the CS. However, arbitrary CSs are unlikely to become conditioned outside the laboratory, because they do not occur often enough with the US to result in an association. Learning under natural circumstances is likely only if the CS has a preexisting relation to the US. Recent studies of sexual conditioning have shown that in contrast to an arbitrary CS, an ecologically relevant CS is resistant to blocking, extinction, and increases in the CS-US interval and results in sensitized responding and stronger second-order conditioning. Although the mechanisms of these effects are not fully understood, these findings have shown that signature learning phenomena are significantly altered when the kinds of stimuli that are likely to become conditioned under natural circumstances are used. The implications of these findings for an ecological approach to the study of learning are discussed.     

Timing of conditioned responses utilizing electrical stimulation in the region of the interpositus nucleus as a CS

A large body of evidence indicates that the cerebellum is essential for the acquisition, retention, and expression of the standard delay conditioned eyeblink response and that the basic memory trace appears to be established in the anterior interpositus nucleus (IP). Adaptive timing of the conditioned response (CR) is a prominent feature of classical conditioning—the CR peaks at the time of onset of the unconditioned stimulus (US) over a wide range of CS-US interstimulus intervals (ISI). A key issue is whether this timing is established by the cerebellar circuitry or prior to the cerebellum. In this study timing of conditioned eyeblink responses established via electrical stimulation of the interpositus nucleus as a conditioned stimulus (CS) was analyzed prior to and following modification of the CS-US interval in well-trained rabbits. Consistent with previous results, learning under these conditions is very rapid and robust. The CR peak eyeblink latencies are initially timed to the US onset and adjust accordingly to lengthening or shortening of the CS-US interval, just as with peripheral CSs. The acquisition of conditioned eyeblink responses by direct electrical stimulation of the IP as a CS thus retains temporal flexibility following shifts in the CS-US delay, as found in standard classical eyeblink conditioning procedures.     

Timing of Conditioned Responses Utilizing Electrical Stimulation in the Region of the Interpositus Nucleus as a CS

A large body of evidence indicates that the cerebellum is essential for the acquisition, retention, and expression of the standard delay conditioned eyeblink response and that the basic memory trace appears to be established in the anterior interpositus nucleus (IP). Adaptive timing of the conditioned response (CR) is a prominent feature of classical conditioning-the CR peaks at the time of onset of the unconditioned stimulus (US) over a wide range of CS-US interstimulus intervals (ISI). A key issue is whether this timing is established by the cerebellar circuitry or prior to the cerebellum. In this study timing of conditioned eyeblink responses established via electrical stimulation of the interpositus nucleus as a conditioned stimulus (CS) was analyzed prior to and following modification of the CS-US interval in well-trained rabbits. Consistent with previous results, learning under these conditions is very rapid and robust. The CR peak eyeblink latencies are initially timed to the US onset and adjust accordingly to lengthening or shortening of the CS-US interval, just as with peripheral CSs. The acquisition of conditioned eyeblink responses by direct electrical stimulation of the IP as a CS thus retains temporal flexibility following shifts in the CS-US delay, as found in standard classical eyeblink conditioning procedures.     

Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat

In delay eyeblink conditioning, the CS overlaps with the US and only a brainstem-cerebellar circuit is necessary for learning. In trace eyeblink conditioning, the CS ends before the US is delivered and several forebrain structures, including the hippocampus, are required for learning, in addition to a brainstem-cerebellar circuit. The interstimulus interval (ISI) between CS onset and US onset is perhaps the most important factor in classical conditioning, but studies comparing delay and trace conditioning have typically not matched these procedures in this crucial factor, so it is often difficult to determine whether results are due to differences between delay and trace or to differences in ISI. In the current study, we employed a 580-ms CS-US interval for both delay and trace conditioning and compared hippocampal CA1 activity and cerebellar interpositus nucleus activity in order to determine whether a unique signature of trace conditioning exists in patterns of single-unit activity in either structure. Long-Evans rats were chronically implanted in either CA1 or interpositus with microwire electrodes and underwent either delay eyeblink conditioning, or trace eyeblink conditioning with a 300-ms trace period between CS offset and US onset. On trials with a CR in delay conditioning, CA1 pyramidal cells showed increases in activation (relative to a pre-CS baseline) during the CS-US period in sessions 1-4 that was attenuated by sessions 5-6. In contrast, on trials with a CR in trace conditioning, CA1 pyramidal cells did not show increases in activation during the CS-US period until sessions 5-6. In sessions 5-6, increases in activation were present only to the CS and not during the trace period. For rats with interpositus electrodes, activation of interpositus neurons on CR trials was present in all sessions in both delay and trace conditioning. However, activation was greater in trace compared to delay conditioning in the first half of the CS-US interval (during the trace CS) during early sessions of conditioning and, in later sessions of conditioning, activation was greater in the second half of the CS-US interval (during the trace interval). These results suggest that the pattern of hippocampal activation that differentiates trace from delay eyeblink conditioning is a slow buildup of activation to the CS, possibly representing encoding of CS duration or discrimination of the CS from the background context. Interpositus nucleus neurons show strong modeling of the eyeblink CR regardless of paradigm but show a changing pattern across conditioning that may be due to the necessary contributions of forebrain processing to trace conditioning.     

Conditioned stimulus informativeness governs conditioned stimulus-unconditioned stimulus associability

In a conditioning protocol, the onset of the conditioned stimulus ([CS]) provides information about when to expect reinforcement (unconditioned stimulus [US]). There are two sources of information from the CS in a delay conditioning paradigm in which the CS-US interval is fixed. The first depends on the informativeness, the degree to which CS onset reduces the average expected time to onset of the next US. The second depends only on how precisely a subject can represent a fixed-duration interval (the temporal Weber fraction). In three experiments with mice, we tested the differential impact of these two sources of information on rate of acquisition of conditioned responding (CS-US associability). In Experiment 1, we showed that associability (the inverse of trials to acquisition) increased in proportion to informativeness. In Experiment 2, we showed that fixing the duration of the US-US interval or the CS-US interval or both had no effect on associability. In Experiment 3, we equated the increase in information produced by varying the C/T ratio with the increase produced by fixing the duration of the CS-US interval. Associability increased with increased informativeness, but, as in Experiment 2, fixing the CS-US duration had no effect on associability. These results are consistent with the view that CS-US associability depends on the increased rate of reward signaled by CS onset. The results also provide further evidence that conditioned responding is temporally controlled when it emerges.     

External inhibition in a goldfish(carassius auratus) classical conditioning situation

Goldfish were classically conditioned with a light as the CS and shock as the US. The UR was a decrease in respiration. After 15 or 60 conditioning trials the fish were tested with novel stimuli (clicks) during the CS-US interval. High and moderate intensity novel stimuli produced a significant decrease in CRs (external inhibition) for fish with 60 conditioning trials (5.5 or 10.5 sec CS-US interval), but not fish with 15 conditioning trials. Low intensity novel stimuli produced no evidence for disinhibition (an increase in CRs). Control groups(e.g., groups with random presentations of the CS and US) showed that the external inhibition for fish with 60 conditioning trials was inhibition of a true CR.     

The decrement in conditioned fear with increased trials of simultaneous conditioning is not specific to the simultaneous procedure

Three experiments using a conditioned punishment paradigm with rat subjects examined the possibility that the nonmonotonic acquisition function previously found to characterize simultaneous conditioning was due to the noninformative nature of the conditioned stimulus (CS). In Experiment 1 the suppressive effects of a CS previously presented with an unconditioned stimulus (US) in a simultaneous and forward (informative) manner were compared following 20 and an additional 60 conditioning trials. Excitatory conditioning similarly diminished with increased trials for both the simultaneous and forward procedures. Experiment 2 employed a between-groups design. Simultaneous, forward, and trace conditioning procedures were compared following 20 or 100 trials. Each of the three 100-trial groups showed less resistance to extinction than their 20-trial counterparts. Experiment 3 determined that the decrement in excitatory conditioning for the 100-trial groups was not due to the greater number of US presentations, per se, but rather to the number of CS-US pairings. The nonmonotonic acquisition function observed with all three conditioning procedures indicated that informational factors were not responsible for the decrement observed in simultaneous conditioning. The pattern of results suggested that subjects receiving extended conditioning trials were better able to discriminate between training and testing.     

Classical conditioning as a nonstationary,multivariate time series analysis: A spreadsheet model

The implementation of the Gallistel (1990) model of classical conditioning on a spreadsheet with matrix operations is described. The model estimates the Poisson rate of unconditioned stimulus (US) occurrence in the presence of each conditioned stimulus (CS). The computations embody three implicit principles:additivity (of the rates predicted by each CS),provisional stationarity (the rate predicted by a given CS has been constant over all the intervals when that CS was present), andpredictor minimization (when more than one solution is possible, the model minimizes the number of CSs with a nonzero effect on US rate). The Kolmogorov-Smirnov statistic is used to test for non-stationarity. There are no free parameters in the learning model itself and only two parameters in the formally specified decision process, which translates what has been leamed into conditioned responding. The model predicts a wide range of conditioning phenomena, notably: blocking, overshadowing, overprediction, predictive sufficiency, inhibitory conditioning, latent inhibition, the invariance in the rate of conditioning under scalar transformation of CS-US and US-US intervals, and the effects of partial reinforcement on acquisition and extinction.     

Pavlovian conditioning of sexual arousal: parametric and background manipulations

Recent studies have shown that a Pavlovian conditioned stimulus (CS) for unconsummated sexual arousal can increase the rate of copulation in the rat. This report includes five experiments examining the effects of parametric manipulations on the conditioned arousal response. Results show that between six and nine trials are necessary for reliable conditioning, but extinction is somewhat slower than acquisition. The function for the CS-US (unconditioned stimulus) interval is quadratic, with a minimum of several minutes required for effective conditioning. In the first three experiments, it appeared that background cues were conditioned as well as the designated CSs, and this was tested explicitly in the last two studies. In one, the effect of background cues was shown by training and testing in different situations; in the second, background cues were shown to be subject to latent inhibition. These results demonstrate the influence of Pavlovian learning in sexual behavior and help to provide the basis for an animal model of the acquisition of deviant sexual arousal in humans.     

Mechanisms of blocking by contextual stimuli

The influence of contextual stimuli on the conditioning and performance of responding to a discrete stimulus was examined in the US preexposure paradigm using both context shift manipulations and a measure of context conditioning. Four groups of rats received both repeated exposure to an electric shock US in one context (Context 1), and repeated nonshocked exposure to a second context (Context 2). Two additional groups of rats received exposure to these contexts, but never received shock presentations. Rats exposed to shock learned to escape from the stimuli of Context 1, but did not escape from the stimuli provided by Context 2. Rats not exposed to shock failed to escape from either context. All rats then received a single CER conditioning session in which four pairings of a 3-min noise CS and shock US were presented. Half the rats received those CS-US pairings in the excitatory Context 1, while the remaining rats received those pairings in the neutral Context 2. Finally, half the rats in each of the CER conditioning treatments received extinction test trials of the noise CS in Context 1, while the remaining rats received those test trials in Context 2. Thus, this design factorially manipulated the presence of excitatory or neutral contextual stimuli during both conditioning and testing of a discrete CS. In comparison with the two groups of rats never preexposed to shock alone, attenuation in acquisition of conditioned suppression observed during test trials occurred only when CER conditioning had been administered in the excitatory Context 1, and this effect was manifested when testing occurred in either the excitatory Context 1 or the neutral Context 2. These results support the model of R. A. Rescorla and A. R. Wagner (1972) (in A. H. Black & W. F. Prokasy (Eds.) Classical Conditioning II, pp. 64–99, New York: Appleton-Century-Crofts) which asserts that contextual stimuli and sicrete CSs compete for limited associative strength supportable by a given US.     

Biological vs experiential factors in phobic conditioning

The present study was performed as a test of phobic conditioning being a case of prepared learning (Seligman, 1971). Skin conductance responses were conditioned in three groups of subjects to either slides of snakes and spiders; electric outlets; or geometric shapes, as conditioned stimuli (CSs) with shock to the forearm as the unconditioned stimulus (UCS). The purpose of the experiment was to compare electrodermal conditioning to potentially phobic CSs, i.e. snakes and spiders, with conditioning to fear-relevant, but non-phobic, CSs, i.e. electric outlets.Each subject saw two pictures, either a snake or a spider; or two different slides of electric outlets; or two different geometric shapes. Only one of the two cues (the CS + ) was immediately followed by the shock-UCS during the acquisition phase. Thus, a differential paradigm was used. There were 4 habituation, 12 acquisition, and 16 extinction trials. The duration of the pictures was 8 sec with an intertrial interval of between 35–45 sec.The results showed reliable effects of conditioning in all three groups during the acquisition phase. Furthermore, a significant interaction during extinction is reported, indicating responses to potentially phobic CSs to be more resistant to extinction than responses to the other two classes of stimuli. It is concluded that the present results favor an interpretation of phobic conditioning in terms of biologically prepared learning.     

Shaking That Icky Feeling: Effects of Extinction and Counterconditioning on Disgust-Related Evaluative Learning

Learned disgust appears to play an important role in certain anxiety disorders, and can be explained by the process of evaluative conditioning, in which an affective evaluative reaction evoked by an unconditional stimulus (US) is transferred to a conditional stimulus (CS). Much remains unknown about how disgust-related evaluative learning can be effectively eliminated. Study 1 of the present investigation examined the effects of extinction on reducing the negative evaluation of a CS that was acquired during disgust conditioning. Participants completed acquisition trials, with a disgusting picture as US and two neutral pictures as CS (CS + was paired with the US; CS- was unpaired), followed by extinction trials ("CS only"; experimental condition) or a filler task (control condition). Extinction trials reduced acquired US expectancy to the CS +, but did not extinguish negative evaluations of the CS +. Study 2 examined the effects of counterconditioning on evaluative learned disgust. After disgust acquisition trials, counterconditioning trials followed in which the CS + was paired with a pleasant US (experimental condition) or a filler task (control condition). Counterconditioning trials reduced acquired US expectancy to the CS + and reduced evaluative conditioned disgust. Implications of the potential differential effects of extinction and counterconditioning on evaluative learning for exposure-based treatment of specific anxiety disorders are discussed.