Pavlovian phenomena in conditioned acceleration—Stimulus summation

Four naive male rats were separately fear-conditioned to two stimuli (light and sound) by pairing these stimuli with shocks. During Sidman avoidance these unreinforced stimuli elicited increases in response rates (conditioned acceleration). In a multiple schedule with light-shock and sound-shock reinforcements in the first component, the rats were tested for summation effects in the second (avoidance) component by presenting the light twice, the sound twice and the compound twice. They were then extinguished by eliminating the shocks in the first component. The effects of compounding were evidenced by: (1) a sizeable and reliable amplitude increase to the compound stimulus during conditioning; (2) a smaller and less consistent decrease in latencies during conditioning in all four subjects; and (3) a greater resistance to extinction for the compound stimulus as measured by mean amplitudes for all four subjects and on six of seven extinction sessions. Latency data during extinction were inconclusive. An additional unexpected finding was what appeared to be a two-factor secondary extinction of the avoidance itself as a result of Pavlovian extinction. The responding in the first four minutes of avoidance was inhibited to such an extent that the number of shocks received during this period increased 700 per cent from the last three conditioning sessions to the first three extinction sessions.     

Hippocampal associative cellular responses: dissociation with behavioral responses revealed by a transfer-of-control technique

Multiunit activity was recorded in the CA3 field of the dorsal hippocampus in freely moving rats during classical conditioning and subsequent presentation of the CS on operant baselines for food reward as well as shock avoidance. Rats were first trained in a nonsignaled bar-pressing-dependent shock omission task and in a food-motivated lever-pressing task (60-s VI). Five sessions with presentations of a previously habituated tone as a CS paired with footshock as a US were then given. Testing was carried out by presenting the CS alone while behavioral responses were maintained by reinforcement in both instrumental tasks on alternate sessions. As expected, the CS induced a marked suppression of lever pressing for food reward and a marked enhancement of bar-pressing for shock avoidance. The analysis of the frequency of multiunit discharges to the CS revealed that the hippocampal cellular responses established during classical conditioning were maintained while two different behavioral responses were exhibited to the CS. The results showed that the associative response of hippocampal neurons may be dissociated from the Pavlovian conditioned responses the CS elicits. They support the hypothesis that hippocampal cellular responses represent a neural index of the acquired CS-US associative representation.     

Classical heart-rate conditioning in the rat: The influence of curare and various setting operations

Conflicting reports concerning the success of classical conditioning of heart rate (HR) in curarized animals led to an experiment using a transfer design in which rats were classically conditioned either under curarized or restrained conditions. These conditions were then reversed for each group, giving a Curarized-Restrained (C-R) and a Restrained-Curarized (R-C) group. Results indicated that curare inhibits the conditional and unconditional HR response both during initial acquisition and after asymptotic levels of a HR CR have been attained. In addition, the C-R group did not acquire a CR during their later non-curarized restrained conditioning sessions, implying an inhibitory transfer from their earlier conditioning under curare. The UCRs during this period were normal for restrained rats. Analogous experimental“setting operations” prior to restrained conditioning were then explored by a second experiment which attempted to replicate the inhibitory transfer effect. The experimental operations investigated included: (1) restrained conditioning to investigate conditioned inhibition possibilities; (2) pseudo-conditioning types of randomized CS and UCS non-paired presentations to investigate associative vs. non-associative explanations; (3) CS-Only presentations to investigate possibilities that curare creates a blockage to the UCS, thus creating an inhibiting habituation to the CS; and (4) a group receiving curarization sessions, but no conditioning, to test the drug-only transfer effects. Results from the first and second experiments together indicated no inhibitory transfer effects under any prior experimental conditions except for those animals receiving classical conditioning while curarized. Only the CS-O group demonstrated any other kind of significant transfer effect; in this case a positive transfer accelerating later conditioning due to prior CS habituation sessions. These findings were discussed within the context of existing reports of curarized conditioning and setting operation effects on later conditioning, and various potential explanations and interpretations were explored.     

Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris)

An experimental group of lemon sharks received 100 daily presentations of light flash as the conditioned stimulus (CS) and electric shock as the unconditioned stimulus (US) in a classical conditioning situation. The conditioned responses (CRs) and unconditioned responses (URs) under observation consisted of extensions of the nictitating membrane. Separate control groups received either (a) no CS or US, (b) CS-alone, or (c) completely random presentations of CS and US. Few CRs occurred in the experimental group at the outset of conditioning, but the percentage of CRs during the second half of the first acquisition session exceeded 95%. Conditioning stabilized above 95% CRs during Acquisition Sessions 3 through 7. These responses could not be attributed to pseudoconditioning, sensitization, or other nonassociative factors. When the experimental group was subsequently given six CS-alone sessions, the course of extinction was gradual. Most results seemed similar to those previously obtained during classical conditioning of the nictitating membrane in rabbits.     

Cardiovascular responses to avoidance conditioning in the dog: Effects of alpha adrenergic blockade

Laboratory dogs were trained to press a response panel to postpone shocks during daily one-hour avoidance conditioning periods. Each dog was also confined in the experimental environment for 5 hours prior to the avoidance periods. Blood pressure and heart rate were monitored continuously during these experiments from chronically indwelling arterial catheters. Extended training resulted in the emergence of a cardiovascular response pattern during the pre-avoidance interval characterized by gradual increases in blood pressure together with decreases in heart rate. Elevations in both blood pressure and heart rate were sustained during the avoidance periods. During sessions in which alpha adrenergic activity was suppressed by phenoxybenzamine, absolute levels of blond pressure were found to be lower than during control (non-drug) sessions, but a progressive rise in blood pressure continued to be observed during pre-avoidance. These results suggest that sustained cardiovascular responses during avoidance periods are associated with activation of the sympathetic nervous system, but that the gradual rise in blood pressure during pre-avoidance is due to other factors.     

Classical Delay Eyeblink Conditioning in in 4- and 5-Month-Old Human Infants

Abstract-Simple delay classical eyeblink conditioning, using a tone conditioned stimulus (CS) and airpuff unconditioned stimulus (US), was studied in cross-sectional samples of 4- and 5-month-old healthy, full-term infants. Infants received two identical training sessions, 1 week apart. At both ages, infants experiencing paired tones and air-puffs demonstrated successful conditioning over two sessions, relative to control subjects who had unpaired training. Conditioning was not evident, however, during the first session. Two additional groups of 5-month-olds received varied experiences during Session 1, either unpaired presentations of the CS and US or no stimulus exposure, fol-lowed by paired conditioning during Session 2. Results from these groups suggest that the higher level of conditioning observed following two sessions of paired conditioning was not the result of familiarity with the testing environment or the stimuli involved but, rather, the result of retention of associative learning not expressed during the first conditioning session.     

Negative reinforcement as shock-frequency reduction

Is a conditioned aversive stimulus necessary in avoidance conditioning? Or is a reduction in the rate of aversive stimulation alone sufficient to generate and maintain an avoidance response? Rats were subjected to an avoidance procedure in which shocks occurred randomly in time, but a response could reduce the overall rate of shock. Fifteen acquisition curves, obtained from 16 animals, showed both immediate and delayed, rapid and gradual increases in response rate; there was no representative acquisition curve. Response rates were directly related to the amount by which the response reduced shock frequency. In extinction, when shock rates were not affected by responding, the response total was inversely related to the amount by which the response had reduced shock frequency during prior conditioning, with as many as 20,000 extinction responses when the shock frequency reduction had been relatively small. Responding on this procedure shows that avoidance conditioning can occur without benefit of either classical exteroceptive stimuli or covert stimuli inferred from the temporal constancies of a procedure. It also shows that reduction in shock rate is alone sufficient to maintain avoidance.     

Signaled avoidance in the eye withdrawal reflex of the green crab

Learning in a signaled avoidance procedure was studied in the eye withdrawal reflex of the green crab, Carcinus maenas. A puff of air to the eye, which causes eye retraction, was used as the unconditioned stimulus (US). A mild vibration on the carapace, which has no effect on untrained animals, was used as a warning (conditioned) stimulus (CS). Eye withdrawal during the CS led to the omission of the otherwise scheduled US. Acquisition was rapid, reaching about 75% avoidance after 30 trials. Extinction occurred slowly over the course of 40 CS-only trials. Yoked controls did not perform as well. The behavior of experimental animals in the avoidance procedure was found to be essentially identical to the performance of animals subjected to a classical conditioning paradigm in which CS responses had no effect on US presentation. Additional groups of animals were subjected to experiments in which (a) avoidance conditioning (60 trials) was followed by classical conditioning (40 trials) or (b) classical conditioning was followed by avoidance. The behavior of these groups was, again, essentially identical. The results suggest that there may be an underlying Pavlovian mechanism for the learned response, although the contribution of an operant process is not excluded. The results expand the range of invertebrate animals in which fundamental conditioning phenomena can be demonstrated, and may provide a neuronal model for learning in a signaled avoidance procedure.     

Conditioned leg movement in the cat with massed trials,trace conditioning,and weak US intensity

Six male cats served as subjects in a classical conditioning experiment designed to assess the development of an overt conditioned response with experimental parameters that had been demonstrated to produce conditioning of neuro-electrical activity in immobilized cats. The subjects were physically restrained by means of an adjustable full-body cast during the experimental sessions which consisted of 75 habituation trials (light flash alone) followed by 225 trials with light and shock paired in a trace conditioning manner, and 75 additional extinction trials (light alone). The subjects were divided into two groups, and three different experimental sessions were given to each on three consecutive days. Group I received low US intensity (18 v) conditioning on the first day, high US (45–85 v) conditioning on Day 2 and pseudoconditioning on Day 3. Group II received the same sessions, but in a pseudoconditioning —high US—low US order. The results indicated that a conditioned leg movement was produced when the CS was paired in a trace conditioning fashion with either the high or low intensity shock US. The development of the conditioned leg movement across trials was found to be very similar to that of the conditioned neural activity in a previous study using comparable stimuli and procedures.     

Suppression of random-ratio and acceleration of temporally spaced responding by the same prereward stimulus in monkeys

A 1-min tone and light signal that preceded two free pellets of food suppressed the random-ratio responding of four rhesus monkeys, but accelerated the same subjects' responding on a differential-reinforcement-of-low-rate schedule in separate sessions. Both schedule-specific interactions occurred during the first presentations of the signal that previously had been paired with food outside the operant sessions. Thus, neither effect was adventitiously produced. In two subjects, both the direction and magnitude of the prereward change in differential-reinforcement-of-low-rate responding appeared related to baseline response rates: the more rapid the baseline responding, the less was the acceleration during the signal. Suppression and acceleration did not appear as dichotomous effects with separate parameters, but as related effects at least partly determined by the characteristics of the baseline operant performance.     

Fear develops to the conditioned stimulus and to the context during classical eyeblink conditioning in rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This twoprocess learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest, a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

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.     

Fear Develops to the Conditioned Stimulus and to the Context during Classical Eyeblink Conditioning in Rats

In classical eyeblink conditioning, non-specific emotional responses to the aversive shock unconditioned stimulus (US), which are presumed to coincide with the development of fear, occur early in conditioning and precede the emergence of eyeblink responses. This two-process learning model was examined by concurrently measuring fear and eyeblink conditioning in the freely moving rat. Freezing served as an index of fear in animals and was measured during the inter-trial intervals in the training context and during a tone conditioned stimulus (CS) presented in a novel context. Animals that received CS-US pairings exhibited elevated levels of fear to the context and CS early in training that decreased over sessions, while eyeblink conditioned responses (CRs) developed gradually during acquisition and decreased during extinction. Random CS-US presentations produced a similar pattern of fear responses to the context and CS as paired presentations despite low eyeblink CR percentages, indicating that fear responding was decreased independent of high levels of learned eyeblink responding. The results of paired training were consistent with two-process models of conditioning that postulate that early emotional responding facilitates subsequent motor learning, but measures from random control animals demonstrate that partial CS-US contingencies produce decrements in fear despite low levels of eyeblink CRs. These findings suggest a relationship between CS-US contingency and fear levels during eyeblink conditioning, and may serve to clarify further the role that fear conditioning plays in this simple paradigm.     

Contextually Based Conditional Discrimination of the Rabbit Eyeblink Response

Rabbits received conditional discrimination training using contextual stimuli to set the occasion for stimulus pairings during eyelid conditioning. Specifically, animals were exposed to either the presence or the absence of an oscillating chamber light throughout the intertrial interval (50 ± 10 s). For half the animals, this light signaled paired presentations of a discrete tone conditioned stimulus (CS) and air puff unconditioned stimulus (US) while darkness signaled presentations of only the tone CS. The remaining animals experienced the opposite contextual relationship to the conditioning stimuli. These trial types occurred pseudo-randomly across a session, with all transitions between contextual settings (i.e., light or dark) taking place immediately at the CS–US offset. Under these conditions, animals successfully utilized the contextual stimuli as conditional cues for differential responding to the shared CS. Moreover, both light and dark were equally effective as discriminative stimuli. A subset of animals received further training in which the contextual contingency was removed by restricting all conditioning to the CS-alone context. Without the contingency in place, subsequent CS presentations (paired and CS-alone) evoked equivalent conditioned responding across three sessions of training. Following the reinstatement of the contextual contingencies, discriminatory responding was immediately observed and returned to previous levels within three sessions. Finally, animals appeared to use the static representation of the conditional cue, rather than the phasic transition between cues, for discriminatory responding. These findings are discussed in terms of current neurobiological models of eyelid conditioning.     

Classical conditioning of goldfish in the shuttlebox

Goldfish trained in a shuttlebox with light as CS and brief shock as US acquire the shuttling response to light whether or not an avoidance contingency is in effect. That the change in behavior produced by the classical procedure is not due merely to sensitization is demonstrated by a discriminative control. The results suggest the usefulness of the shuttlebox for the study of classical conditioning in goldfish and call into question the instrumental interpretation of the change in behavior produced by the avoidance procedure.     

Compounding discriminative stimuli controlling free-operant avoidance

The performances of three rats were stabilized on a multiple schedule that maintained responding by a free-operant avoidance schedule during independent presentations of tone and light. The simultaneous absence of these stimuli signalled shock-free periods and controlled response cessation. Subsequently, test sessions were administered consisting of independent presentations of each stimulus and these stimuli compounded (tone-plus-light). During an extinction test, additive summation was observed to the compounded stimuli, i.e., more responses were emitted to the compound than to either tone or light. During a series of 28 maintenance-test sessions in which the shock schedule remained operative, the compounded stimuli produced a generally enhanced response rate and fewer pauses terminating with shock than either single stimulus condition. These results extend the generality of free-operant additive summation to responding maintained by aversive control. In addition, a comparison of the present study with previous experiments reporting additive summation of positively reinforced responding indicates that similar variables—rate and aversive differences between training stimulus conditions—should be considered in accounting for response distributions during stimulus compounding when responding is controlled by either positive or negative contingencies.     

Analysis of treatments to alleviate forgetting in rats

Two experiments with rats investigated the effectiveness of prior-cuing treatments for alleviating forgetting of aversive conditioning. The aim was to see which retrieval cues would be most effective within different contexts. Experiment 1 examined the contexts of classical fear conditioning and instrumental avoidance training. The results indicated that the response components were sufficient to reinstate avoidance training, whereas the unconditioned stimulus (US) was most effective for classical fear conditioning. In Experiment 1, the reinforcer per se was ineffective in reinstating instrumental avoidance training. Experiment 2 manipulated the training context and found that the US could be made an effective prior-cuing treatment for instrumental training if classical conditioning components were more prevalent during training. These results are interpreted to mean that a "critical context" must be reinstated by the cuing treatment if this treatment is to promote retrieval of the memory.     

Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning

Previous functional magnetic resonance imaging (fMRI) studies have characterized brain systems involved in conditional response acquisition during Pavlovian fear conditioning. However, the functional neuroanatomy underlying the extinction of human conditional fear remains largely undetermined. The present study used fMRI to examine brain activity during acquisition and extinction of fear conditioning. During the acquisition phase, participants were either exposed to light (CS) presentations that signaled a brief electrical stimulation (paired group) or received light presentations that did not serve as a warning signal (control group). During the extinction phase, half of the paired group subjects continued to receive the same treatment, whereas the remainder received light alone. Control subjects also received light alone during the extinction phase. Changes in metabolic activity within the amygdala and hippocampus support the involvement of these regions in each of the procedural phases of fear conditioning. Hippocampal activity developed during acquisition of the fear response. Amygdala activity increased whenever experimental contingencies were altered, suggesting that this region is involved in processing changes in environmental relationships. The present data show learning-related amygdala and hippocampal activity during human Pavlovian fear conditioning and suggest that the amygdala is particularly important for forming new associations as relationships between stimuli change.     

An experimental analysis of the extinction-induced response burst

The occurrence, time course, and repeatability of response rate increases following the onset of extinction, the extinction burst, were studied in three experiments. Nine pigeons were exposed to at least 5 cycles of 5-session blocks of conditioning followed by 8-session blocks of extinction. In different experiments, conditioning sessions either were a fixed-ratio (FR) or variable-ratio (VR) schedule, and transitions from the last conditioning session in each cycle to the first extinction session were conducted between or within sessions. A single response rate increase occurred when overall response rates were considered. Restricting analyses to the first minute of extinction sessions sometimes revealed increases in response rates, although this finding was inconsistent. The frequency and magnitude of these increases differed across exposures to extinction both across and within pigeons. Additionally, how responding during extinction was measured (i.e., the level of analysis) influenced whether increases above baseline levels were observed. These results suggest that the extinction burst may be influenced by the manner of transition to extinction and the way in which early extinction responding is measured. Under the best conditions, the extinction burst does not appear to be a ubiquitous effect of extinction.     

Instrumental to Pavlovian transfer: Learning about response-reinforcer contingencies affects subsequent learning about stimulus-reinforcer contingencies

Two experiments examined the interaction between response-reinforcer (R-S) and stimulus-reinforcer (S-S) learning. In both experiments, three groups of rats were exposed to escapable, yoked inescapable, or no shocks. All groups were then exposed to either two or four sessions of truly random control (TRC) conditioning (Experiment 1) or to an excitatory conditioning procedure (Experiment 2) in which the shock US occurred with either moderate or low probability. Excitatory strength of the CS was assessed during extinction by a conditioned emotional response (CER) test. Inescapably shocked rats conditioned less than did their escapably shocked and nonshocked partners under all TRC conditions of Experiment 1, but only conditioned less than their partners in Experiment 2 when exposed to the moderate CS-US contingency for four sessions. These results provide a clear demonstration of transfer between instrumental training and Pavlovian excitatory conditioning and thus, support the influence of learning about R-S contingencies upon subsequent learning about S-S contingencies. Both a contextual blocking interpretation and an expansion of the learned helplessness theory were discussed as possible explanations of this transfer.