Blocking and unconditioned response diminution in human classical autonomic conditioning

This paper summarizes the results of three experiments on blocking and unconditioned response diminution in human SCR conditioning. Recent theories of conditioning propose that reduced processing of the unconditioned stimulus due to conditioning results in reduced unconditioned response magnitude and in blocking of conditioning of a second conditioned stimulus when it is in compound with the previously conditioned stimulus. In these experiments, clear evidence of diminution of the unconditioned response was obtained in all three studies, but blocking was found only in the third study, which employed a within-subject design and in which the blocking was observed only after at least one extinction trial on both the blocked and nonblocked stimuli. Order of testing was not a factor in this delayed blocking effect. These results do not support the view that blocking occurs because of reduced processing of the unconditioned stimulus in the unconditioned response diminution sense.     

Acquisition of the classically conditioned eyeblink response in humans over the life span

Human subjects ranging in age from 18 to 85 years underwent classical conditioning of the eyeblink response to a tone conditioned stimulus (CS) and an air-puff unconditioned stimulus (UCS). There was a decline in percentage of conditioned responses with age. This decline was most noticeable in subjects over age 50. These conditioning deficits were not due to age-related changes in sensitivity to the tone CS or the air-puff UCS, nor could the conditioning deficits be attributed to an age-related decline in general cognitive abilities or to changes in spontaneous blink rates. The results are discussed in terms of using the classically conditioned eyeblink in humans in conjunction with the classically conditioned nictitating membrane response in rabbits as a model system for studying the neurobiology of age-related conditioning deficits.     

The Topography of Sexually Conditioned Behaviour: Effects of a Trace Interval

In a trace conditioning procedure, subjects were presented with a 30-sec conditioned stimulus (CS) followed by a 30-sec trace interval. Delayed conditioning consisted of a 60-sec CS presentation followed by an unconditioned stimulus (US). Although conditioning developed with both procedures, the topography of the conditioned response differed. Sexual conditioned approach was evident in all of the subjects during the presentation of the CS. Traceconditioned subjects moved away from the area where the CS had been presented during the trace interval but remained closer to the CS location than did an unpaired control. This reduction in the spatial specificity of the conditioned response was interpreted from a behaviour systems perspective. The trace interval presumably increased the perceived separation between the CS and the US and therefore elicited conditioned behaviour less specifically directed towards the CS.     

Attenuation of age-related conditioning deficits in humans by extension of the interstimulus interval

Young (17-22 years) and older (61-86 years) persons underwent classical conditioning of the eye-blink response to a tone conditioned stimulus (CS) and an airpuff unconditioned stimulus (UCS) at 1 of 3 interstimulus intervals (ISIs; 400, 650, and 900 ms). As in a previous study, older subjects conditioned more slowly and emitted fewer conditioned responses at the optimal 400-ms ISI. At longer ISIs, however, this age-related disruption of classical conditioning was attenuated. These differences in conditioning were not due to nonassociative factors, such as sensitivity to the tone CS or airpuff UCS or to differences in spontaneous blink rate, nor were they due to differences in general cognitive abilities. The results are discussed in terms of the role of temporal relationships between stimuli in conditioning across the life span.     

Conditioned taste aversion with sucrose and tactile stimuli in the pond snail Lymnaea stagnalis

A new form of taste aversion conditioning was established in the pond snail Lymnaea stagnalis. An associative memory, lasting 24h, was produced in the pond snail with 20 pairings of 100 mM sucrose as the conditioned stimulus (CS) and mechanical stimulation to the head as the unconditioned stimulus (UCS). Animals exposed to reverse pairings of the CS and UCS failed to learn the association. The learning was characterized by a shift in the response to the UCS from a whole-body withdrawal response to the cessation of feeding behavior.     

Autoshaping the pigeon's gape response: acquisition and topography as a function of reinforcer type and magnitude.

The pigeon's key-pecking response is experimentally dissociable into transport (head movement) and gape (jaw movement) components. During conditioning of the key-pecking response, both components come under the control of the conditioned stimulus. To study the acquisition of gape conditioned responses and to clarify the contribution of unconditioned stimulus (reinforcer) variables to the form of the response, gape and key-contact responses were recorded during an autoshaping procedure and reinforcer properties were systematically varied. One group of 8 pigeons was food deprived and subgroups of 2 birds each were exposed to four different pellet sizes as reinforcers, each reinforcer signaled by a keylight conditioned stimulus. A second group was water deprived and received water reinforcers paired with the conditioned stimulus. Water- or food-deprived control groups received appropriate water or food reinforcers that were randomly delivered with respect to the keylight stimulus. Acquisition of the conditioned gape response frequently preceded key-contact responses, and gape conditioned responses were generally elicited at higher rates than were key contacts. The form of the conditioned gape was similar to, but not identical with, the form of the unconditioned gape. The gape component is a critical topographical feature of the conditioned key peck, a sensitive measure of conditioning during autoshaping, and an important source of the observed similarities in the form of conditioned and consummatory responses.     

The Adaptive Significance of Sexual Conditioning: Pavlovian Control of Sperm Release

Male quail received Pavlovian conditioning trials that consisted of placement in a distinctive experimental chamber (the conditioned stimulus) paired with the opportunity to copulate with a female (the unconditioned stimulus). For control subjects, exposures to the conditioned and unconditioned stimuli were unpaired. After four and six trials, each subject was placed in the experimental chamber with a probe stimulus that included some of the visual cues of a female's head and neck. Pavlovian conditioning increased how much time subjects spent near the probe stimulus. Conditioned subjects also released greater volumes of semen and greater numbers of spermatozoa than the control subjects. Significant differences were not obtained in serum testosterone levels or in other measures of sperm quality. These results demonstrate that sexual Pavlovian conditioning can affect reflexes involved in sperm release and thereby modulate reproductive fitness.     

Context-specific conditioning in the conditioned-emotional-response procedure

In 3 experiments, rats were used to investigate the conditions that influence the transfer of a conditioned emotional response from 1 context to another. The subjects experienced training in 2 contexts on each day. In Experiment 1, subjects received a single conditioning trial with a different target stimulus in each of the 2 contexts. Conditioned responding was found to be more vigorous when the target was presented subsequently in the context in which conditioning had taken place than when it was presented in the other context. Experiments 2 and 3 confirmed these results and also showed that neither the unconditioned response evoked by the target stimulus nor the conditioned response acquired after multiple training trials showed evidence of context specificity. Possible reasons for the difference in outcome between single-trial and multitrial conditioning procedures are discussed.     

Excitatory conditioning of individual Drosophila melanogaster

Testing individual animals from a heterogenic population of Drosophila melanogaster, we demonstrate conditioning of the proboscis extension reflex. The presentation of paired (conditioning) stimuli produced (a) an increase in the average number of conditioned responses over trials, (b) measured differences in performance levels among individual subjects, and (c) a sex difference, with more males conditioned than females, and those that did did so more quickly. The presentation of unpaired (control) stimuli produced significantly lower average levels of acquisition responding and a change in the distribution of individual response patterns. Neither central excitatory state nor sensitization induced by the conditioned or unconditioned stimuli directly affected the conditioned response, whereas unconditioned stimulus preexposure adversely affected performance levels. Presenting the unpaired (extinction) stimuli after conditioning produced less of a decline in responding than did an extinction procedure with removal of the unconditioned stimulus. With the ability to identify individual differences in acquisition and extinction patterns, and given the relatively large number of individuals that can be tested simultaneously on the automated stimulation apparatus, it is now possible to make precise behavioral measurements on samples large enough for the behavior-genetic analysis of D. melanogaster with conditioning as the phenotype.     

Conditioned suppression by a stimulus associated with nalorphine in morphine-dependent monkeys

Three rhesus monkeys, physically dependent on morphine, were trained to press a lever for food on a fixed ratio of 10 responses. A tone, initially a neutral stimulus, was aperiodically presented every third or fourth session, 5 min before and after the intravenous injection of nalorphine, a morphine antagonist which produces an immediate withdrawal syndrome in morphine-dependent monkeys. After several sessions, conditioned suppression of food-lever response rate was observed. Conditioned bradycardia, emesis, and excessive salivation also occurred. In 40 to 45 sessions the conditioned suppression of food-lever response rate and the conditioned autonomic changes were extinguished by presenting pairings of a tone and saline injection. The monkeys were then reconditioned by presenting the tone aperiodically, every third or fourth session, 5 min before and after the intravenous injection of nalorphine. Results were similar to the initial conditioning sessions. Two rhesus monkeys not dependent on morphine were stabilized on a food schedule similar to that used for the first three monkeys. These monkeys showed no change in food-lever response rate during or after nalorphine injections.     

A pitfall for the expectancy theory of human eyelid conditioning

Two simple eyeblink conditioning experiments with random intermittent reinforcement schedules were performed. In Experiment 1, subjects had to rate their expectancy for an unconditioned stimulus (US) on a seven-level scale prior to each trial. As anticipated, expectancy for US increased with a successive conditioned stimulus (CS) alone, and decreased with successive CS-US pairings. However, Experiments 1 and 2 showed that the frequency of eyeblink conditioned responses (CRs) evolved in a direction opposite to that of expectancy changes: CRs increased, whereas expectancy for US decreased, and vice versa. The possible effect of sensitization on eyeblink response was ruled out by the lack of a run effect in an unpaired control group in Experiment 2. These results tend to disconfirm the expectancy theory of conditioning. Although they were explicitly predicted by the conventional “strength” theory of conditioning, an alternative interpretation is proposed within a cognitive framework.     

A comparison of neuronal reactions during classical and instrumental conditioning under similar conditions

During the elaboration of an instrumental reflex, it is not obligatory to use a conditioned stimulus, which signals the necessity to generate an instrumental reaction in order to receive reinforcement. However, the presence of a conditioned stimulus simplifies analysis of instrumental reaction, which in this case is the response to the conditioned stimulus. On the other hand, it is necessary to distinguish between instrumental and classical conditioning, since in both cases the response to a conditioned stimulus increases. We studied neuronal analogs of classical and instrumental conditioning in the identified neurons responsible for the defensive closure of the pneumostome in the Helix mollusk under the same conditions. During classical conditioning, a mollusk received punishment after a tactile stimulus. During instrumental conditioning, a mollusk received punishment when an identified neuron did not generate an action potential in response to a tactile stimulus. The appearance of a painful stimulus did not depend on the generation or failure of a spike in the related control neuron. Another tactile stimulus, which was never paired with an unconditioned stimulus, was used as a discriminated stimulus. We also compared the behavior of such identified neurons during pseudoconditioning. The experiments were carried out in a semi-intact preparation. We examined how responses to the tactile and painful stimuli changed during different forms of training. It was shown that the dynamics of neuronal responses to a conditioned tactile stimulus were much more complex during instrumental conditioning and consisted of several phases. Throughout a learning session, neural system consecutively acquired information as to which kind of learning was presented, whether a reaction of the neural system must be generated or inhibited and which instrumental reaction is correct. We have demonstrated that response to a painful stimulus during classical conditioning decreases after short-term initial increase. However, during instrumental learning, the neurons controlling instrumental action remained highly sensitive to the unconditioned stimulus. Meanwhile, foreign neurons decreased their responses to the unconditioned stimulus. We may tentatively conclude that classical and instrumental paradigms are fundamentally different at the cellular level.     

UCS revaluation and conditioning models of acquired fears

Recent developments in the study of Pavlovian conditioning in humans have suggested that the strength of a conditioned response (CR) is affected not only by associative processes that link the conditioned stimulus (CS) with the unconditioned stimulus (UCS), but also by processes which lead the individual to revalue the UCS itself. These latter processes can frequently lead to dramatic changes in CR strength independently of any experience with the CS-UCS contingency. This paper discusses a number of ways in which UCS revaluation can be effected in human subjects, and discusses their implications for conditioning models of acquired fears.     

Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation.

Rabbits received 0 to 450 exposures of a tone conditioned stimulus (CS) prior to classical defensive conditioning of the nicitating membrane response based on an infraorbital eye shock unconditioned stimulus. Tone preexposure resulted in retarded conditioning in normal rabbits. This latent inhibition effect was not present in animals with bilateral dorsal hippocampectomy produced by aspiration. Control animals with bilateral neocortical and callosal aspiration lesions demonstrated a latent inhibition effect similar to that shown by normal nonoperated animals. The failure of CS preexposure to retard conditioning in hippocampal rabbits was not due to differences in threshold of the conditioned response to the CS or to differences in response mechanisms as determined by tests of habituation and dishabituation of the unconditioned response. A subsequent experiment employed combined-cue summation tests to confirm the fact that preexposure did not endow the tone with conditioned as well as latent inhibitiory properties. Finally, tests of stimulus generalization along the auditory frequency dimension indicated flatter relative gradients for hippocampals than for nonoperated controls, with cortical controls in between. These findings were discussed in terms of Douglas' model of hippocampal function.     

Classical conditioning of hippocampal theta patterns in the rat.

Electrical stimulation (88 HZ) of the lateral hypothalamus elicited a sustained theta response at hippocampal recording sites of rats immobilized with succinylcholine. By pairing this unconditioned stimulus with a 10-sec presentation of a light, conditioned theta responses were demonstrated in as few as 40 trials. Spectral analysis of hippocampal bioelectric patterns during acquisition, extinction, and reconditioning indicated that the earliest change as a result of conditioning is a loss of power in EEG frequency below 8 HZ, followed by the development of a peak at 8 HZ with further conditioning. Extinction was associated with an increase in power in the frequencies below 8 HZ. When the conditioned rats were tested in the absence of the neuromuscular blocking agent, the conditioned stimulus elicited a theta response that was associated with slow motor activity on 70% of the trials.     

Reflex conditioning in a spinal man.

A man with a completely transected spinal cord and a spastic neurogenic bladder was conditioned to void upon the presentation of an external stimulus. A classical conditioning paradigm was employed in which strong abdominal shock (unconditioned stimulus) was paired with an initially neutral mild electrical stimulation of the thigh (conditioned stimulus; CS). After the pairing trials, a reliable conditioned response of urination was elicited by the CS alone. The conditioned response did not extinguish over time, and the procedure left the bladder with clinically safe residual amounts of urine. Practical implications of the conditioning technique for the treatment of spastic neurogenic bladder conditions in spinally injured patients are discussed, as is the theoretical significance of conditioning at the reflex level in the absence of cortical involvement.     

Pavlovian second-order conditioned analgesia

Three experiments with rat subjects assessed conditioned analgesia in a Pavlovian second-order conditioning procedure by using inhibition of responding to thermal stimulation as an index of pain sensitivity. In Experiment 1, rats receiving second-order conditioning showed longer response latencies during a test of pain sensitivity in the presence of the second-order conditioned stimulus (CS) than rats receiving appropriate control procedures. Experiment 2 found that extinction of the first-order CS had no effect on established second-order conditioned analgesia. Experiment 3 evaluated the effects of post second-order conditioning pairings of morphine and the shock unconditioned stimulus (US). Rats receiving paired morphine-shock presentations showed significantly shorter response latencies during a hot-plate test of pain sensitivity in the presence of the second-order CS than did groups of rats receiving various control procedures; second-order analgesia was attenuated. These data extend the associative account of conditioned analgesia to second-order conditioning situations and are discussed in terms of the mediation of both first- and second-order analgesia by an association between the CS and a representation or expectancy of the US, which may directly activate endogenous pain inhibition systems.     

Pavlovian conditioning with ethanol and lithium: effects on heart rate and taste aversion in rats

Rats received paired injections of either ethanol or saline as the conditioned stimulus and lithium chloride as the unconditioned stimulus (US) in a Pavlovian differential conditioning paradigm. Lithium chloride evoked a large deceleration in heart rate (80-100 beats per minute) as an unconditioned response. As a result of 10 conditioning trials, the substance paired with LiCl elicited a lower average heart rate than that elicited by the unpaired substance. Moreover, animals that received ethanol-LiCl injections subsequently were more averse to the taste of ethanol than animals receiving saline-LiCl pairings. However, there were no differences in ethanol's ability to serve as the US to induce an aversion to a novel flavor solution (i.e., the Avfail phenomenon was not observed). The overall pattern of results underscores the value of using multiple indexes of learning in drug-drug conditioning paradigms.     

One-trial conditioned suppression: effects of instructions on extinction

Two experimental groups of undergraduate volunteers received a single Pavlovian conditioning trial consisting of a paired presentation of a tone conditioned stimulus (CS) and a shock unconditioned stimulus (UCS). Control groups received either the CS alone or the UCS alone. Subjects from one experimental group were subsequently instructed that they would not receive further shocks, while the other experimental group received no such instructions. The CS alone was then presented once to all four groups while subjects were engaged in a button-pressing task maintained by slide reinforcement. During the latter phase, rate of button-pressing was measured. Classically conditioned suppression of button-pressing was obtained in the noninstructed experimental group but not in the instructed group. The results demonstrate that suppression can be a sensitive index of Pavlovian conditioning in humans but question the use of conditioned suppression as an adequate experimental analog of clinically observed anxiety-motivated behavior.     

Consequences of response-contingent change in unconditioned stimulus intensity upon the rabbit (Oryctolagus cuniculus) nictitating membrane response.

In a between-groups design, an instrumental contingency was superimposed on classical conditioning of the rabbit nictitating membrane response. Subjects were exposed to a tonal conditioned stimulus (CS) and, if no conditioned response (CR) occurred, a 5.0-ma. paraorbital electric shock unconditioned stimulus (US). USs of 5.0, 3.3, 1.7, and 0.0 ma., respectively, were contingent on occurrence of a CR in the CS-US interval for subjects in the 4 groups of the experiment. The group exposed to contingent US omission differed from the other 3 groups in percentage CR, onset latency, amplitude, and 2 indices of CR form, and those 3 groups generally did not differ significantly among themselves on these dependent variables. Results were interpreted to be contrary to "law of effect" formulations of classical conditioning.