Amygdalar unit activity during three learning tasks: eyeblink classical conditioning, Pavlovian fear conditioning, and signaled avoidance conditioning

Neural activity in central and basolateral amygdala nuclei (CeA and BLA, respectively) was recorded during delay eyeblink conditioning, Pavlovian fear conditioning, and signaled barpress avoidance. During paired training, the CeA exhibited robust learning-related excitatory activity during all 3 tasks. By contrast, the BLA exhibited minimal activity during eyeblink conditioning, while demonstrating pronounced increases in learning-related excitatory responsiveness during fear conditioning and barpress avoidance. In addition, the relative amount of amygdalar activation observed appeared to be related to the relative intensity of the unconditioned stimulus and somatic requirements of the task. Results suggest the CeA mediates the Pavlovian association between sensory stimuli and the BLA mediates the modulation of instrumental responding through the assignment of motivational value to the unconditioned stimulus.     

The effects of task type and task requirements on the dissociation of skin conductance responses and secondary task probe reaction time

Although task-irrelevant events elicit smaller skin conductance responses (SCRs) than do task-relevant events, secondary task probe reaction time (RT) is often slower during the former. Three experiments (N = 48 in each) examined the effects of task demands, instructions, and stimulus discriminability on this dissociation effect. SCRs were larger to task-relevant stimuli in all experiments regardless of experimental manipulation. Subjects in Experiment I counted either all tones of one pitch (high/low group) or longer-than-usual tones of one pitch (longer group). There was more RT slowing during task-irrelevant tones at a 250-ms probe position in the high/low group and at a 150-ms probe position in the longer group. Experiment 2 employed differential Pavlovian conditioning in which the offset of task-relevant stimuli (CS+) coincided with the onset of a shock stimulus. Half the subjects were told which stimulus would be followed by shock (information group), whereas the others received no information (no-information group). Increased RT slowing during CS? was restricted to the no-information group. Experiment 3 employed visual conditioned stimuli that were easy or difficult to discriminate. RT slowing at 4,000 ms was greater during CS+, whereas there was a tendency for more RT slowing during CS? at 150 ms. There was no effect for CS discriminability. The results suggest that during both simple discrimination and during Pavlovian conditioning, task-irrelevant stimuli are more actively processed than task-relevant stimuli within the first 250 ms of stimulus presentation.     

Effects of early experiences on shock-and illness-induced passive avoidance behaviors

Rats were either handled, shocked, or unmanipulated during the preweaning period or during the 21 days immediately following weaning. At maturity animals were tested in 2 passive avoidance situations. Half the animals were first tested in an illness-induced taste aversion situation using sour water as the CS and different doses of cyclophosphamide as the US. The remaining animals were first tested in a 1-trial passive avoidance situation using a “step-through” apparatus and a single electric shock. Early experience had no effect on the development of a taste aversion at any dosage of cyclophosphamide. Prior conditioning of a taste aversion did influence performance in the step-through avoidance situation. Fewer of these previously conditioned animals attained the training criterion and, within this previously conditioned population, the handled groups displayed less “emotional” behavior than the controls. Response latencies in the shock-induced passive avoidance test did not differentiate between handled and shocked animals. Animals manipulated prior to weaning had consistently shorter latencies than the unmanipulated controls.     

Involvement of the telencephalon in spaced-trial avoidance learning in the goldfish (Carassius auratus)

Goldfish (Carassius auratus) received escape-avoidance training in a shuttle-response situation at a rate of a single trial per day. Widely spaced training evaluates the ability of a discriminative stimulus to control an avoidance response in the absence of stimulus carry-over effects from prior recent trials. In Experiment 1, master goldfish exhibited significantly faster avoidance learning than yoked controls. The results suggest that the shuttle response was instrumentally acquired. Experiment 2 demonstrated a significant deficit in the acquisition of avoidance behavior following ablation of the telencephalon. The implications of spaced-trial, telencephalon-dependent avoidance learning, as demonstrated in these experiments for the first time, are discussed in the context of comparative research on instrumental learning in goldfish. These results provide further support for the hypothesis that the fish telencephalon contains an emotional system that is critical for fear conditioning.     

Avoidance learning, Pavlovian conditioning, and the development of phobias

This paper examines the role of Pavlovian conditioning in the acquisition, maintenance and elimination of human phobias. Because many conceptualizations of human fears and phobias are based on data from studies of avoidance learning in animals, we first review theories of avoidance. Our conclusion is that none of the extant theories provides an adequate account of avoidance learning, and we propose a model of avoidance that involves Pavlovian, but not instrumental learning. We then analyse critically arguments that Pavlovian conditioning plays only a small role in the aetiology of fears. Finally, the paper examines the implications of a conditioning model of avoidance for the study of human fears and phobias.     

Paradoxical sleep at selective times following training is necessary for learning

Rats were trained in a two-way shuttle shock avoidance task, 20 trials per day for 5 consecutive days. In Experiment 1, groups were subjected to selective paradoxical sleep deprivation (PSD) for daily 4 hour periods. It was found that only PSD applied between 9–12 hours or 17–20 hours after the daily training sessions resulted in acquisition deficits. These vulnerable time periods coincided with polygraphically observed PS increases above normal levels following identical training procedures in previous studies. In Experiment 2, animals were only allowed PS during the 9–12 hour and 17–20 hour post training time “windows” observed in Experiment 1. For the remaining time each day, they were subjected to PSD. Acquisition was found to be unimparied, despite this severe treatment. However, any other equivalent length PSD regime which overlapped with either of the time “windows” resulted in severe retardation of task acquisition. Results were believed to provide strong support for the sleep-learning hypothesis.     

Naloxone induces multiple effects on aversive Pavlovian conditioning in rabbits

A series of experiments examined the effects of intravenous naloxone treatment on aversive Pavlovian conditioning of eye-blink and heart rate responses, and related unconditioned behaviors, in rabbits. Naloxone treatment before testing attenuated bradycardiac orienting responses to tones used as conditioning stimuli. Naloxone also attenuated conditioned bradycardia when administered either before or after training sessions, but it potentiated conditioned bradycardia during extinction of discriminative conditioning. Naloxone did not influence acquisition or extinction of discriminative eye-blink conditioning or somatic or cardiac responses to shocks used as unconditioned stimuli, but it did decrease locomotor activity. Naloxone treatment immediately after training sessions facilitated acquisition of eye-blink responses. It was concluded that naloxone influences aversive Pavlovian conditioning in more than one way: (a) During training, it appears to alter reception and processing of signals but does not affect subsequent development of somatic responses to the Pavlovian conditioning contingency. (b) After training sessions, naloxone apparently affects consolidation of both somatic and autonomic conditioning. (c) Naloxone also appears to delay extinction of Pavlovian conditioning; this effect may similarly involve changes in a stimulus-processing mechanism or in memory functions, but it apparently does not involve changes in somatomotor responsitivity.     

In utero cocaine, discriminative avoidance learning with low-salient stimuli and learning-related neuronal activity in rabbits (Oryctolagus cuniculus)

Daily injections of cocaine administered to pregnant rabbits (Oryctolagus cuniculus) throughout gestation were associated with neural and behavioral changes during development and in adulthood, including altered neuron structure and function in areas receiving dopaminergic projections and retarded Pavlovian eyeblink conditioning with low-salient conditional stimuli. Studies of discriminative avoidance learning have shown changes in learning-related cingulothalamic neuronal activity, but no behavioral learning impairment in cocaine-exposed offspring. Here, low-salient stimuli were used during discriminative avoidance conditioning. Impairments early in behavioral acquisition were found, as well as alterations of anterior cingulate and medial prefrontal cortical, medial dorsal thalamic, and amygdalar neuronal response profiles and learning-related neuronal activity. These results elucidate the neural processes, impaired by prenatal cocaine, that support conditioning with low-salient stimuli.     

Conditionnement operant avec renforcement thermique chez le rat nouveau-né

In previous experiments, we studied the acquisition of instrumental locomotor responses reinforced by thermal stimuli, in one to ten-day-old rats. In these tasks, there was a precise topographic relation between the behavior to be conditioned and the reinforcement. In the experiment reported in the present paper, one to eight-day-old rats were tested in an operant conditioning task, where the operant (OP) was a non locomotor behavior, the raising of the head. At each day of age, two paired groups were compared: a “contingent” (C) and a “non contingent” (NC) group. Each OP (satisfying an amplitude criterion) of a C rat was reinforced by the application of a 30–35°C air-stream during ten seconds. The NC rat of the same pair received the same number of air-streams during the session, but these stimuli were unrelated to its behavior. The duration of the session was ten minutes. Mean frequency of OP was higher in C than in NC groups, at one, two, six, seven and eight day of age. Absence of significant differences between C and NC groups at three, four and five days of age could be due to the competition between OP and the emerging locomotor behavior.     

The effect of unconditional stimulus modality and intensity on blink startle and electrodermal responses

Attentional accounts of blink facilitation during Pavlovian conditioning predict enhanced reflexes if reflex and unconditional stimuli (US) are from the same modality. Emotional accounts emphasize the importance of US intensity. In Experiment 1, we crossed US modality (tone vs. shock) and intensity in a 2 × 2 between-subjects design. US intensity but not US modality affected blink facilitation. In Experiment 2, we demonstrated that the results from Experiment I were not due to the motor task requirements employed. In Experiment 3, we used a within-subjects design to investigate the effects of US modality and intensity. Contrary to predictions derived from an attentional account, blink facilitation was larger during conditional stimuli that preceded shock than during those that preceded tones. The present results are not consistent with an attentional account of blink facilitation during Pavlovian conditioning in humans.     

Plasma glucose levels and leverpress avoidance versus escape behaviors in rats.

The relationship between performance in an avoidance conditioning paradigm and the plasma glucose levels of Sprague-Dawley rats was examined in two experiments. In Experiment 1 we investigated whether glucose levels varied with the animal's relative success at acquiring the avoidance task. Results indicated that animals classified as avoiders (60% avoidance and above) had lower glucose levels than animals classified as escapers (30% avoidance and below). In Experiment 2 we looked at whether glucose levels showed within-subject changes with avoidance acquisition. Results demonstrated that glucose levels showed reductions if an animal learned the avoidance response. Subjects that did not learn the response showed no such reduction. Such results suggest that the physiological response to stress is attenuated by acquisition of successful coping behaviors that exercise control over the onset of aversive events.     

Effects of conditioned stimulus pre-exposure on human electrodermal conditioning to fear-relevant and fear-irrelevant stimuli

The effects of conditioned stimulus (CS) pre-exposure and fear-relevance of the CS on human Pavlovian electrodermal conditioning were investigated. A differential delayed conditioning paradigm was used with a CS-unconditioned stimulus (US; shock) interval of 8 s. In Experiment 1, 64 subjects were randomized into four groups, two of which received fear-relevant stimuli and the other two fear-irrelevant stimuli. Half of the subjects were pre-exposed to the to-be-CSs and the other half to two not-to-be-CSs, with 15 exposure of each stimulus. During acquisition, subjects received 8 reinforced and 8 nonreinforced CS+ and CS- trials, and during the extinction phase 15 nonreinforced trials of each CS. Pre-exposure to the to-be-CSs retarded conditioning for the first and second interval anticipatory responses (FIRs and SIRs); that is, a latent inhibition effect was demonstrated, although the results for the FIR were inconclusive. The expected effects of fear-relevance were not revealed. Experiment 2 addressed the question whether the long pre-exposure period interfered with the frequently observed "preparedness effect" of higher resistance to extinction to fear-relevant stimuli. The design was similar to that of Experiment 1, but for half of the subjects the acquisition phase was initiated immediately after a short rest period, and for the other half acquisition started after an extended rest period, equal to the duration of the pre-exposure phase in Experiment 1. Twenty extinction trials of each CS were presented. A reliable difference in arousal in terms of spontaneous fluctuations was produced by the rest periods, but although differential conditioning was observed, no effect of fear-relevance was seen during extinction.     

Retained elements of early avoidance training and relearning of forgotten operants

In a series of 7 experiments we investigated the possibility that juvenile rats show long-term retention for aspects of early avoidance training and that these retained elements serve to reinforce relearning of the forgotten operants. Rats trained in active or passive avoidance at 23–25 days of age demonstrated the typical juvenile forgetting effect relative to adults after a 28-day interval. However, both juveniles and adults demonstrated marked reductions in locomotor activity prior to retraining which were specific to the apparatus and not dependent on the opportunity to perform an operant during initial training. Juvenile animals given a reminder exposure plus footshock 27 days after training, then single daily nonshock trials (Days 28–30), showed decreasing crossover latencies across days if trained in active avoidance and increasing latencies if trained in passive avoidance. This reappearance of task-appropriate crossover latencies was evident in previously trained juveniles only. Finally, young animals' demonstrated change in crossover latency is associated with subsequent superior acquisition performance, and this change depends upon the presentation of the test trials for its appearance. We suggest that the amelioration of “infantile amnesia” associated with the present procedures is a learning process motivated by Pavlovian components of training which are retained well, by juveniles and adults alike, over intervals typical of ontogeny of memory research.     

The impact of reinforcement density on response differentiation in configural discrimination problems

Two human Pavlovian conditioning experiments investigated the impact of reinforcement density (the number of reinforced trials divided by the total number of trials) on discrimination learning. Experiment 1 used a negative patterning problem (A+, B+, AB-) and Experiment 2 used a positive patterning problem (A-, B-, AB+). In both experiments, reinforcement density varied across four levels. Response differentiation between reinforced and non-reinforced stimuli was linearly related to the decrease in reinforcement density. Responses to nonreinforced stimuli did not differ between the four groups in either experiment. In contrast to this, responses to reinforced stimuli were considerably more pronounced in conditions with lower reinforcement density. For negative patterning, this replicates and extends similar observations from other species. For positive patterning, this is a finding that has not yet been reported in other experiments. The results are in agreement with the comparator hypothesis (Miller & Matzel, 1988) and with Wagner's (1981) "standard operating procedures" (SOP) model.     

Leg flexion conditioning in the rat: its advantages and disadvantages as a model system of age-related changes in associative learning

Twelve- and 28-month-old Fischer 344 rats of both sexes received five 60-trial sessions of Pavlovian conditioning in which the CS was a 75 dB, 10,000 Hz tone, and the US was a 0.5-mA, 0.5-sec duration footshock. Right foreleg flexion was measured as the conditioned response (CR). Other animals received a random sequence of unpaired tones and footshock and served as pseudoconditioning control groups. Interstimulus intervals (ISIs) of 1.5 and 3.5 sec were studied. The longer ISI resulted in higher rates of responding in both the conditioning and pseudoconditioning groups. However, with the exception of the young males, all animals showed significantly higher levels of responding in the conditioning groups. Females also showed faster acquisition and higher levels of responding than males. A significant sex by age by sessions interaction occurred, suggesting that old males may be somewhat retarded in acquiring the leg flexion CR compared to the other groups of animals. Old males were also slower to reach a criterion of 5 successive CRs than either young males or young or old females.     

Effects of Momentary Changes in Arousal on Discriminative Autonomic Classical Conditioning

Relative to an intermediate arousal level, effects of stimulus-controlled increases and decreases in arousal were examined during discriminative autonomic conditioning. After matching subjects to psychophysiologically-indexed arousal criteria, three experimental and two control groups of 14 persons each were formed. Experimental groups received both high arousal training consisting of aversive conditioning with a discrete stimulus and low arousal training involving paired presentations of muscle biofeedback relaxation and a different cue. Formation of stimulus controlled arousal responses was assessed using heart rate, muscle, and electrodermal criteria. During discriminative conditioning, one experimental group received all conditioned stimuli compounded with high arousal cues, while another group received conditioned stimuli/low arousal cue compounds. The third experimental group received conditioned stimuli/neutral cue compounds. Electrodermal and digital pulse volume conditioning data indicated significantly greater conditioning associated with neutral cue manipulations. High arousal cue compounds resulted in conditioning superior to that displayed by low arousal cue compounds. Control groups data suggested that results were not due to simple transfer or physical cue properties alone.     

Selective resistance to approach: A precursor to fear responses to an alarm call in great tit nestlings Parus major

The reactions of 10-day-old great tit nestlings to 3 auditory stimuli were studied. The stimuli, presented on a series of feeding occasions, were (1) the species' “seeet” alarm call, (2) a song strophe of the great tit, and (3) a song strophe of the tree-creeper (Certhia familiaris). In contrast to earlier findings in studies of older nestlings, these younger nestlings did not respond to the alarm call with cessation of begging. However, a significant differential effect of the alarm call was demonstrated when the conditioning rates for the nestlings' begging response to each of the 3 stimuli were determined. Thus, conditioning was significantly slower to the alarm call than to the other stimuli. The results agree with the general conception that responses to species-specific calls develop gradually during early ontogenesis. Thus fear responses to the alarm call, such as cessation of begging and “freezing,” which are elicited in newly fledged young, are preceded by weaker aversive tendencies that are not obvious from observations of the nestlings' behavior in nature. It is suggested that the nestlings' exposure to contrasting auditory stimulation–their own begging call and the parental feeding call–constitutes the experiential base for withdrawal responses to the “seeet” call.     

Interoception,conditioning, and fear: The panic threesome

The present article aims to illustrate and review evidence on how associative learning involving interoceptive stimuli (interoceptive conditioning) can lead to changes in physiological, emotional, and perceptual outcomes. We first outline a functional perspective on Pavlovian conditioning and provide a general introduction and historical background on interoceptive conditioning as a special instance of Pavlovian conditioning. Next, biological and learning accounts of panic disorder are discussed, followed by an analysis of which stimuli and responses may be most promising to model learning that is relevant to panic disorder. Finally, studies on interoceptive fear conditioning with respiratory stimuli are reviewed and discussed, and future directions are outlined.     

Profiling, mimicking and masking the flavor of a selected rodenticide

In Experiment 1, rats drank strychnine solution followed by an injection of LiCl. Generalization of learned strychnine avoidance to 4 non-toxic flavors was then assessed. Additional conditioning and generalization trials followed until 24 flavors had been presented. In Experiment 2, rats were conditioned to avoid individual flavors, or flavor mixtures concocted on the basis of avoidance generalization observed in Experiment 1. Tests followed for generalization of learned avoidance from the simple flavors to the mixtures, from the mixtures to the simple flavors, and from either to strychnine. In Experiment 3, two concentrations of NaCl were mixed with strychnine or one of the flavors (SOA) used in the previous experiments. These stimuli, as well as SOA alone, strychnine alone, and each of the NaCl concentrations, were presented to rats during conditioning. Generalization followed, as in the previous experiments. In Experiment 1, strychnine avoidance generalized to 'bitter' flavors (ps less than 0.01). In Experiment 2, avoidance of flavor mixtures generalized more strongly to strychnine than did learned avoidance of simple flavors (ps less than 0.01). In Experiment 3, NaCl masked or otherwise suppressed the 'bitter' flavor of strychnine or SOA insofar as no groups conditioned with a 'bitter'-salt mixture generalized avoidance to 'bitter' alone (ps less than 0.01). Rats are therefore capable of recognizing the flavor components of strychnine. Moreover, when these components are mixed in proportion to the degree of generalized avoidance, a mimic (either in terms of flavor characteristics or perceived intensity) of strychnine is obtained. Avoidance learning appears useful in the development of rodenticide baits and pre-bait formulations.     

Blocking, unblocking, and overexpectation of fear: a role for opioid receptors in the regulation of Pavlovian association formation

Injection of the opioid receptor antagonist naloxone facilitated acquisition of fear to contextual and auditory conditioned stimuli (CSs) in Experiments 1A and 1B. Experiment 2 showed that prior conditioning to a distinctive context blocked conditioning to an auditory CS. Blocking of CS fear was prevented by administrations of naloxone or increases in footshock intensity. Blocking of CS fear was facilitated by decreases in footshock intensity in a naloxone-reversible manner. Experiment 3 showed that compound conditioning of two CSs, each previously and separately paired with shock, produced overexpectation of fear that was reversed by naloxone. These results are consistent with a role for opioid receptors controlling Pavlovian association formation by regulating the discrepancy (lambda - SigmaV) described by R. A. Rescorla and A. R. Wagner (1972).