CER suppression, passive-avoidance learning, and stress-induced suppression of drinking in the Syracuse high- and low-avoidance strains of rats (Rattus norvegicus)

The Syracuse strains of Long-Evans rats were selectively bred for good (SHA) or poor (SLA) avoidance learning in a two-way shuttle box, which resulted in a phenotypic difference that is correlated with behavior patterns indicative of emotional reactivity, SLA animals showing evidence of greater emotional reactivity than SHA animals. The first three experiments examined conditioned suppression of bar pressing and compared paired and unpaired conditioned- and unconditioned-stimulus presentations to evaluate the influence of conditioning versus primary aversive stimulation on baseline responding. SLA animals acquired conditioned suppression faster than SHA animals and also showed greater suppression of baseline responding than SHA animals. In Experiment 4, SLA animals learned a passive-avoidance task faster than SHA animals. In Experiment 5, SLA animals showed greater stress-induced suppression of drinking a weak quinine solution than SHA animals. These data are consistent with the hypothesis that SLA animals are more emotionally reactive than SHA animals.     

Rats (Rattus norvegicus) selectively bred to differ in avoidance behavior also differ in response to novelty stress, in glycemic conditioning, and in reward contrast

The behavior of the Syracuse high avoidance (SHA) and Syracuse low avoidance (SLA) rats, selectively bred by Brush (F. R. Brush, J. C. Froehlich, & P. Sakellaris, 1979, Behavior Genetics, 9, 309-316) to differ in avoidance behavior, was examined in several different tasks. The SLA rats showed a greater elevation in plasma glucose when exposed to a novel environment; after 7 days of exposure to this environment there was evidence of habituation in the SHA rats but not in the SLA rats; the SHA rats showed a hyperglycemic conditioned response in a glycemic conditioning procedure, the SLA rats showed no evidence of conditioning but had higher overall levels of plasma glucose; both strains showed reliable successive negative contrast effects in consummatory behavior when shifted from 32 to 4% sucrose, but the contrast was larger in the SLA rats; the administration of chlordiazepoxide eliminated negative contrast in the SLA rats but had no effect on contrast in the SHA rats; and the SLA rats were reliably heavier than the SHA rats. The behavioral differences were considered in the context of differences in emotional reactivity between the two strains.     

The Syracuse strains,selectively bred for differences in active avoidance learning,may be models of genetic differences in trait and state anxiety

The derivation of the Syracuse high- and low-avoidance strains is described. The behavioral characterization of the high- and low-avoidance phenotypes is summarized and it is concluded that the SLA/Bru strain is best described as having higher state and trait anxiety than their SHA/Bru counterparts. Although the behavioral covariates of the high- and low avoidance phenotypes are consistent, the covariation of the endocrine system normally thought to be involved in stress, is anomalous. The SLA/Bru rats, which are behaviorally more anxious than the SHA/Bru animals, show hypertrophy of the adrenal glands but reduced synthesis and release of the stress-related corticosterone than the SHA/Bru animals. This dissociation of the behavioral and endocrine measures of anxiety appears to be genetic, since a selective genetic analysis, involving F2 and high and low backcross segregating generations, indicates that both the behavioral and endocrine covariates cosegregate with the avoidance phenotypes. These data suggest that the expected association of behavioral and endocrine measures of anxiety is correlational, not causal.     

Conditioned taste and taste-potentiated odor aversions in the Syracuse high- and low-avoidance (SHA/Bru and SLA/Bru) strains of rats (Rattus norvegicus).

Syracuse high- and low-avoidance Long-Evans rats (Rattus norvegicus; SHA/Bru and SLA/Bru) were selectively bred for good and poor active-avoidance learning. However, SLA/Bru animals are superior to SHA/Bru rats in conditioned suppression and passive avoidance learning. In this experiment, saccharin taste and almond odor were the components of a compound conditioned stimulus (flavor) in an illness-induced aversive conditioning paradigm. SLA/Bru rats (n = 17) showed stronger conditioned flavor, taste, and odor aversion than did SHA/Bru animals (n = 18). Unselected Long-Evans rats (n = 18) were intermediate between the selected strains. SLA/Bru and Long-Evans rats showed taste-potentiated odor aversions in this experiment, whereas SHA/Bru animals did not. The results provide evidence that genetic factors, as exemplified by the different strains, are importantly involved in the mechanisms underlying interoceptive and exteroceptive aversive conditioning.     

Immobility as an avoidance response, and its disruption by drugs

Much of the available literature on avoidance behavior is based on responses which require the animal to run, lever-press, or to make some active response to avoid noxious stimulation. The purpose of Experiment I reported in this paper was to determine whether animals can learn to sit or stand motionless in order to escape or avoid electric shock. Five experimental rats were given escape-avoidance training, while five yoked control animals received electric shocks without any response-related contingency. It was shown that an immobility avoidance response, as distinct from the unconditioned “freezing” response to shock, can be trained. The results of Experiment II (30 rats) revealed that this response is more readily acquired at higher shock intensities than at lower ones, provided escape by jumping is prevented at the high shock intensities. The effects of six doses of each of three drugs on the immobility avoidance response were studied in Experiment III (13 rats). Methylphenidate, chlorpromazine, and imipramine all produced a decrement in the immobility response, but the pattern and amount of the effects of the three drugs were quite different, one from the other. The implications of these findings for a general theory of avoidance behavior and for drug screening are discussed.     

Successive negative contrast in one-way avoidance learning in rats

In three experiments, successive negative contrast was examined in one-way avoidance learning. Reward magnitude in first (pre-shift) and second (post-shift) phases was manipulated by time spent in the safe compartment. Experiment 1 demonstrated that when time in the danger compartment was held constant, a group shifted from a large reward--30 sec spent in the safe compartment--to a small reward--1 sec--showed poor performance and longer response latency than a group conditioned with the small reward in both phases. Experiment 2 replicated this effect with a less intense shock and also demonstrated that a group shifted from large to small reward performed more poorly than a group exposed to large reward--30 sec--in both phases. Finally, Experiment 3 showed that changes in intertrial interval, defined as total time spent in the safe compartment and the danger compartment before the onset of the warning signal, were not responsible for this contrast effect. These results suggest that time spent in a safe place can act as appetitive incentive during one-way avoidance learning.     

Determinants of fear over the course of avoidance learning

Most theorists have explained attenuation of fear over the course of avoidance learning by assuming that fear extinguishes with repeated nonreinforced avoidance trials. Experiment 1 replicates the finding that rats trained to a criterion of 27 consecutive avoidance responses (CARs) show less fear during the CS than rats trained to a criterion of 3 or 9 CARs. This attenuation of fear cannot, however, be accounted for by simple Pavlovian fear extinction, because yoked partners receiving the exact same pattern of CSs and USs did not show this attenuation and did not differ from yoked partners receiving only reinforced CS presentations. Experiment 2 found that feedback from the master avoidance learner's response is sufficient to produce this attenuation in yoked animals; “control” per se is not necessary. Several possible explanations are discussed regarding the mechanism underlying this role of feedback in diminishing fear of the CS in the avoidance learning context.     

Successive positive contrast in one-way avoidance learning

The main finding of these experiments was a positive contrast effect in one-way avoidance learning. Experiment 1 showed that increasing safety time during one-way avoidance training led to improved performance, surpassing that of a control group that had received the high reward (safe time) from the beginning of training. Experiment 2 showed that a similar positive contrast effect occurred when the time spent in the danger compartment before the onset of the warning signal was shortened. These results suggest that time spent in a safe context acts as a reinforcer of the avoidance response; however, its incentive value depends not only on its duration, but also on the length of the time spent in the danger compartment before the onset of the signal. Overall, results also suggest that the avoidance response is a mixture of flight (motivated by fear) and approach (to a safe place) behaviour. The specific weight of the flight or approach component may be a function of the time and the amount of activation of each emotional state (fear or relief) due to opponent homeostatic compensatory processes that occur in the danger and safe compartments during one-way avoidance learning.     

One-way characteristic performance of rats under two-way signaled avoidance conditions

In Experiment 1, the conflict in a two-way active avoidance was reduced by allowing rats to avoid one of two levels of shock by running onto a safe platform which covered one half of the grid floor. Performance characteristics of one-way avoidance were obtained regardless of the shock intensity. Groups with no platform showed poor performance. Experiment 2 suggested that the facilitatory effect of the platforms was not due to the cue associated with platform removal. These results suggest that (a) rats can quickly learn to enter a spatially aversive location, (b) fast avoidance learning may be obtained in a two-way setting, and (c) rats seem capable of selective association of environmental and aversive stimuli.     

Measurement of fear of the conditioned stimulus and of situational cues at several stages of two-way avoidance learning

In Experiment 1, subjects were trained in a signaled two-way avoidance task to a criterion of either 2, 10, or 20 consecutive avoidance responses. Subsequently, they were allowed to escape, in the absence of shock, from one compartment of the avoidance apparatus to an adjacent safe box. For one group at each criterion level, the conditioned stimulus (CS) was presented during these trials; for another group, it was not (NCS). The rate and level of learning of the escape response were taken to reflect the amount of fear of the CS and situational cues present at the end of avoidance training for the CS groups and the amount of fear of the situational cues alone for the NCS groups. Under the CS condition, all groups learned equally well; under the NCS condition, learning occurred only in the two-criterion group. This pattern of results suggests that, as avoidance training continued, differential reinforcement led to the formation of a discrimination so that a substantial amount of fear was elicited by the CS plus situational cues but only a minimal amount by the situational cues alone. Such a loss of fear of situational cues would, according to effective reinforcement theory, serve to maintain or even increase reinforcement as avoidance training progressed. The results of Experiment 2, by ruling out some alternative explanations, supported the interpretation that the learning of the instrumental escape response in the first experiment was based on prior fear conditioning.     

Reaction to punishment, reflectivity, and passive avoidance learning in extraverts

Passive avoidance learning occupies a central role in accounts of disinhibited behavior, ranging from psychopaths' persistent criminality (Hare 1970) to extraverts' gregariousness (Gray, 1972). To explore the mechanism underlying passive avoidance deficits, we assessed the relation of extraversion, neuroticism, and response latency after punishment to passive avoidance learning by using two successive go/no go discrimination tasks. The tasks were designed to examine two aspects of subjects' reactions to punishment: response speed on trials immediately following punishment (Experiment 1) and time to terminate punishment feedback between successive trials (i.e., reflectivity; Experiment 2). Consistent with previous findings, the results of Experiment 1 showed that extraverts commit more passive avoidance errors than introverts do (Newman, Widom, & Nathan, 1985) and fail to pause following punished errors (Nichols & Newman, 1986). In Experiment 2, only neurotic extraverts displayed this pattern of performance differences. In both experiments, longer pausing following punishment predicted better learning from punishment for both introverts and extraverts. These results suggest that, in the presence of salient cues for reward, extraverts' characteristic reaction to punishment interferes with processing punished errors and may contribute to their more general propensity for impulsive, nonreflective action.     

Rapid acquisition of discrete-trial lever-press avoidance: effects of signal-shock interval

Acquisition of discrete-trial lever-press avoidance learning was studied in three experiments. Experiment I compared a new training procedure, which produces rates of lever-press avoidance learning comparable to those obtained in shuttle boxes, with a “conventional”, less efficient training procedure. A factorial design was used to compare continuous versus intermittent shock and a long-variable versus a short-fixed signal-shock interval. Learning was best in the groups trained with the long and variable interval and poorest in those trained with the short and fixed interval. Type of shock had no effect. Experiment II separated the effects of duration from those of variability of the signal-shock interval. Fixed and variable intervals of 10 and 60 sec were tested and duration was the only significant factor. Experiment III addressed the effect of the differential opportunity to avoid provided by long signal-shock intervals by varying this interval from 10 to 60 sec in 10-sec steps. Only the 10-sec group showed slow acquisition relative to the others. Analysis of avoidance response latencies showed that the distributions for all groups were positively skewed and that skewness increased with increasing duration of the signal-shock interval. At intervals longer than 20 sec, the animals made progressively less use of their increased opportunity to respond. The data do not support the opportunity-to-respond interpretation of the effects of duration of signal-shock interval and suggest that some type of inhibitory process may block lever-press avoidance learning at intervals as short as 10 sec. The significance of these findings for species-specific defense reaction and preparedness theories was emphasized.     

Acquisition and extinction of signaled avoidance as a function of intermittent reinforcement

Signaled, shuttle-box avoidance responding in female rats of the Fischer₃₄₄ strain was examined as a function of four separate contingencies of intermittent reinforcement. In Experiment 1, when avoidance responses during acquisition were reinforced 25% of the time with prompt CS termination, animals responded equally often during acquisition and significantly more often during extinction than animals who received such reinforcement on a 100% schedule. Similar results were found under a trace procedure in Experiment 2 when avoidance responses were reinforced 25% of the time with informational feedback stimuli. In contrast, during Experiment 3, when animals were shocked on only 25% of the trials on which they failed to respond, the level of avoidance responding during both acquisition and extinction was significantly less than it was when animals were shocked on a 100% schedule. Comparable results were found in Experiment 4 when avoidance responses during acquisition averted shock on only 25% of the trials. Thus, intermittent reinforcement contingencies involving response-contingent feedback stimuli and shock have differential effects on avoidance responding during both acquisition and extinction trials under the signaled avoidance procedure.     

Pavlovian processes and response competition as determinants of avoidance response-prevention effects

Two experiments investigated the facilitation of avoidance extinction by exposure to lengthy (5-sec) shock during avoidance response prevention. In Experiment 1, animals exposed to light only or to light-shock pairings during response prevention showed equal facilitation of extinction relative to shock-only animals or to animals receiving no response prevention. Preshock rearing, directly antagonistic to the avoidance response, developed for shocked animals during response prevention and persisted during extinction for light-shock animals. Immediately before extinction, half of each group was permitted a single escape from a light-shock compound by means of the response previously required for avoidance. The only effect was upon the extinction performance of light-shock animals. Rearing was eliminated and extinction responding increased to a level far above that for any of the other animals. Experiment 2 demonstrated that the shock-only treatment affected the extinction performance and rearing of nonescape and escape animals in a manner entirely equivalent to the effects of the light-shock treatment of Experiment 1, provided stimulus conditions (light absent) were the same for all experimental phases. Thus, lengthy shock during avoidance response prevention simultaneously leads to the acquisition of competing behavior and enhances control by a warning signal or contextual stimuli over the avoidance response. Implications for the CS-only response-prevention treatment and the transfer of aversive control are discussed.     

The fearless avoiders: Comparison of various strains of rats in an active avoidance task

The effect of exploratory activity and emotional reactivity on the acquisition of active avoidance learning was assessed in rats. Four strains of rats selectively bred for a high or low degree of either of the two traits (Maudsley emotionally reactive animals, Maudsley emotionally non-reactive animals, high rearers, and low rearers) and a control strain (randombred animals) took part in the experiment. Significant differences were found between strains in the number of animals showing active avoidance behaviour. Emotional reactivity was shown to facilitate active avoidance behaviour and so did, unexpectedly, a low degree of exploratory activity. An attempt was made to explain the latter result in terms of differences in channel capacity between high and low exploring animals and the ensuing differences in attention focus on the relevant stimulus for the test situation.     

Evidence for expectancy as a mediator of avoidance and anxiety in a laboratory model of human avoidance learning

A laboratory model was developed to study human avoidance learning. Participants could avoid an electric shock signalled by a 5-s conditioned stimulus (CS) by pressing one of a set of response buttons. Self-reported shock expectancy and skin conductance were recorded during a subsequent 10-s interval before shock. Shock expectancy declined when the correct avoidance response was learned and returned when the response was unavailable. Learning transferred to another shock CS. Parallel effects were observed on skin conductance once performance anxiety was controlled by requiring responding on all trials. Learning was faster when the Pavlovian contingencies were trained before introduction of the instrumental response. The results support a cognitive model of anxiety in which performance of an avoidance response reduces expectancy of an aversive outcome and thereby reduces anxiety.     

Evidence for expectancy as a mediator of avoidance and anxiety in a laboratory model of human avoidance learning

A laboratory model was developed to study human avoidance learning. Participants could avoid an electric shock signalled by a 5-s conditioned stimulus (CS) by pressing one of a set of response buttons. Self-reported shock expectancy and skin conductance were recorded during a subsequent 10-s interval before shock. Shock expectancy declined when the correct avoidance response was learned and returned when the response was unavailable. Learning transferred to another shock CS. Parallel effects were observed on skin conductance once performance anxiety was controlled by requiring responding on all trials. Learning was faster when the Pavlovian contingencies were trained before introduction of the instrumental response. The results support a cognitive model of anxiety in which performance of an avoidance response reduces expectancy of an aversive outcome and thereby reduces anxiety.     

Postacquisition injection of tetrodotoxin into the parabrachial nuclei elicits partial disruption of passive avoidance reaction in rats.

The recent discovery that post-trial functional blockade of the parabrachial nuclei by intracerebral injection of 10 ng tetrodotoxin (TTX) disrupts acquisition of conditioned taste aversion (CTA) (Ivanova & Bures, 1990a,b) has prompted attempts to ascertain the role of this structure in other types of inhibitory learning. In Experiment 1, rats with implanted parabrachial cannulae were trained in a step-through avoidance task and received bilateral TTX (2 x 10 ng) immediately after the acquisition trial; they displayed significantly weakened avoidance of the shock compartment 2 days later. In Experiment 2, rats were anesthetized with pentobarbital (50 mg/kg) immediately after passive avoidance acquisition and received parabrachial TTX 15 min later; whereas anesthesia alone left the passive avoidance reaction (PAR) unaffected, TTX elicited similar disruption as in unanesthetized animals. In Experiment 3, TTX was injected in anesthetized animals 0, 1, 2, or 4 days after PAR acquisition. The amnesic effect was significant when the acquisition-TTX delay had been prolonged to 24 but not to 48 or 96 h. Since CTA is disrupted by reversible blockade of parabrachial nuclei and of the adjacent reticular formation elicited up to 4 days after acquisition (Ivanova & Bures, 1990b), PAR seems to be impaired to a lesser degree and for a shorter time than CTA by similar TTX treatment.     

Continuous punishment of free-operant avoidance in the rat

Three groups of albino rats were trained under a free-operant avoidance (Sidman) procedure with equal shock-shock and response-shock intervals. After stable performance was achieved, the animals were concurrently exposed to a brief electric shock after each response. The procedures were as follows: Punishment Schedule I: punishment shock was introduced at an intensity approximately one quarter that of avoidance shock; increments of nearly this same size were made as stable performance was achieved at succeeding punishment shock intensities. Punishment Schedule II: punishment shock was introduced at approximately one-half the intensity of avoidance shock; after stable performance, punishment shock was increased to the same intensity as avoidance shock. Punishment Schedule III: punishment shock was introduced and maintained at the same intensity as avoidance shock. Punishment was continued for all groups until one of two suppression criteria was attained. All animals made fewer responses and received more avoidance shocks as a function of increasing punishment shock. Half of the animals under Punishment Schedule I required punishment shock higher than avoidance shock to meet their assigned suppression criterion. A comparison of all procedures showed that suppression was greater when punishment shock was initially at high intensity.     

The effects of estradiol on avoidance learning in ovariectomized adult rats

The present study examined the effects of ovariectomy and subsequent estradiol replacement on learning in young adult rats using a set of instrumental avoidance paradigms differing in the nature and extent of prior experience in the learning context. Thus, one group of animals was placed directly into avoidance learning (AV). A second group was trained on an appetitive task first, and then transferred into the aversive context (AP-AV). The third group was exposed to the training context without any specific appetitive response requirement, and then required to learn an active avoidance response (Context-AV). We found that estradiol (OVX+E) impaired avoidance acquisition in all cases relative ovariectomized controls (OVX). In contrast, while avoidance learning is improved following appetitive training or context exposure in both OVX+E and OVX animals, the OVX+E animals profit to a greater extent from the appetitive or context experience than do the OVX controls. We suggest that this difference may be due to enhanced attentional processes or improved hippocampal processing of contextual factors. Thus, estradiol negatively influences simple associative avoidance learning in ovariectomized rats, but appears to promote positive transfer.