Retention of massed vs distributed response-prevention treatments in rats and a revised training procedure.

Two experiments were conducted to estimate the retention of response-prevention effects using massed vs distributed treatments in a model of animal avoidance-learning. In Exp. I, 120 rats were trained to avoid shock in a one-way platform avoidance apparatus. Groups received response-prevention treatment or nontreatment in a 36-min. massed session or in several sessions distributed over a four-day period. In Exp. II, 160 rats were given two trials of escape training in a one-way shuttle box. Groups received response-prevention treatment or nontreatment in a 24-min. session of massed or distributed treatments delivered in one day. Subjects in both studies were tested using a passive-avoidance paradigm immediately following treatment, 24 hours later, and 30 days later. Analysis showed that response-prevention treatments were effective in reducing avoidance behavior and there were no significant differences in retention of avoidance associated with massed vs distributed response-prevention treatments. Implications for animals and humans are discussed, and researchers are encouraged to change from a criterion training procedure to an escape procedure since the latter is a closer analogue to the human condition.     

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.     

The effects of preexposure to a learning apparatus

ICR mice were given exposure to a one-way shuttle apparatus until locomotor activity had been habituated. When compared with nonexposed animals, the exposed animals displayed superior shuttle avoidance learning. Animals exposed to both the apparatus and the CS did not differ from the nonexposed group. It was concluded that preexposure to the learning apparatus facilitated acquisition, while preexposure to the apparatus in the presence of the CS did not. The relationship between this effect and habituation was considered.     

Between-trial transporting of animals: A methodological consideration

The advantages of the one-way avoidance situation are numerous. However, to start a. new trial, the E is confronted with the additional problem of transporting S, usually by hand, from the nonshock compartment to the shock compartment. Two experiments were run in which the performance of a group transported between trials by hand was compared with a group transported by a specially designed box. The main finding in both experiments was that between-trial handling of Ss markedly retards the number of responses occurring during extinction. The importance of removing the handling variable from experiments was discussed.     

Avoidance responding in pigeons

Four pigeons were trained in a one-way shuttle box avoidance situation. Three of the birds met the criterion of 90% avoidances; the fourth, although frequently avoiding successfully, was too erratic to meet the criterion. Avoidance responding in two of the birds was subsequently extinguished, showing that the response was true avoidance, and not escape from the buzzer warning stimulus. In Experiment 2, the three birds that had met criterion in Experiment 1 were trained in a two-way avoidance task, and all three met the criterion of 90% avoidances. The shuttle box therefore provides a rapid and reliable method of obtaining avoidance performance in pigeons.     

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.     

Open-field and avoidance behavior after neostriatal lesions in male and female rats.

The behavioral effects of lesions of the anterodorsal or posteroventral parts of the caudate-putamen were studied in adult male and femle rats that were gonadectomized or left untreated prior to brain surgery. Anterodorsal (ADC) lesions consistently impaired acquistion of one-way avoidance behavior and tended to interfere with the development of a two-way avoidance response; comparable effects were observed in gonadectomized and intact animals of both sexes. By contrast, ADC lesions increased activity in the open field only in intact females and increased rearing only in ovariectomized females. Posteroventral caudate (PVC) lesions caused transient aphagia and adipsia in both sexes but did not consistently affect open-field activity or the acquistion of one-way avoidance responses by either sex. These lesions profoundly impaired acquistion of shuttle box avoidance responses by intact males. By contrast, castrated males and intact and ovariectomized females with PVC lesions avoided normally in the shuttle box. The present results suggest that localization of behavioral functions within the striatum differs with the sex of the subject, in part because of activational effects of gonadal hormones.     

Avoidance conditioning with shock contingent upon the avoidance response

Rats learned either a lever-press response, a shuttle response or a one-way crossing response, which produced one immediate shock but was instrumental in avoiding five identical shocks scheduled to occur later. These responses were acquired both with and without support of an escape contingency. These results support shock-frequency reduction as a sufficient condition for the acquisition and maintenance of avoidance.     

Extinction of avoidance in rats: response availability and stimulus presentation effects

A conditioned a versive stimulus presented in prolonged, continuous fashion is said to be flooded. Using a two-way shuttle avoidance task. Polin (1959) found that animals allowed to respond to flooded stimuli extinguish faster than animals prevented from responding to discrete stimuli of equal total duration. But, as Shearman (1970) noted, the CS presentation and response availability factors were confounded. He arranged them factorially, in a 2 × 2 design, again utilizing two-way avoidance, but found no differences between any of the experimental groups, although all groups extinguished faster than a regular extinction control group, the only group for which CS termination was response-contingent. Since there is evidence from one-way avoidance studies that response prevention facilitates extinction of avoidance with CS exposure held constant (Shipley et al., 1971). we repeated the Shearman design, using a one-way avoidance paradigm, and including a group for whom the aversive CS would be presented in discrete trials at increasing intensities. A separate aspect of the present investigation concerned the measurement of a fear response as well as the avoidance response. Results of several investigations have shown (e.g. Coulter et al. 1969; Linton et al.. 1970) that avoidance behaviour can be extinguished without the extinction of fear. It was thought useful to assess the generality of this result, since in two-factor theory, fear and avoidance are related.Two supplementary experiments replicated important conditions of the initial one, while examining whether response prevention and response non-availability have similar effects (II), and the relation between the fear test and the test for extinction (III).     

Sidman avoidance in the fish

Goldfish trained in a shuttle box under conditions in which changing compartments postponed shock for 20 sec showed a substantial, negatively accelerated increase in rate of crossing. That the avoidance-contingency was responsible for the change in behavior is suggested by the fact that no significant increase in rate of crossing appeared in control animals which were paired with the experimentals and shocked whenever the experimental animals were shocked; there is some evidence, indeed, that the control animals were handicapped in their subsequent adjustment to the avoidance condition. The introduction of a warning stimulus (light) in the last 5 sec of the response-shock interval decreased the rate of crossing in the first 15 sec and increased the rate of crossing in the last 5 sec. Reducing the shock-shock interval from 20 sec to 2.5 sec had no marked effect. The results are compared with those obtained in analogous experiments with higher animals.     

Task complexity as a factor in eliciting heterosis in mice: aversively motivated behaviors.

Three inbred strains of mice (A/J, DBA/2J, and C57BL/6J) and their six reciprocal F1 hybrids were tested in activity levels before and after shock, inhibitory avoidance, one-way avoidance, and shuttle avoidance. In the activity and inhibitory situations the hybrids generally exhibited an intermediate pattern of inheritance. In the one-way avoidance task complete dominance was the rule, whereas in the shuttle task overdominance was apparent in all the hybrid strains. Overdominance was found to be more evident in tasks requiring increased versatility of associative processes. It is suggested that when the task involves relatively simple contingencies or reflexive behaviors, increased versatility is not necessary and consequently the hybrid advantage is not apparent. When the task involves integrative capacities, the hybrid advantage emerges.     

Methylphenidate, amygdalectomy, and active avoidance performance in the rat

Amygdalectomized and control rats were given 400 active avoidance training trials in a shuttle box. Control animals received 0, 4, 8, or 16 mg/kg of methylphenidate throughout acquisition. Amygdalectomized animals were given the first 200 trials without drug, followed by 200 trials with drug. The administration of methylphenidate produced an abrupt and large improvement in performance in the amygdalectomized animals. One month after acquisition under the drug, retraining without drug revealed a significant retention effect for the three amygdaloid-drug groups relative to the nondrug-amygdaloid group. These results indicate that although amygdalectomy impairs the performance of avoidance responses, it does not prevent the learning or retention of such responses. Since methylphenidate appears to act primarily on dopaminergic mechanisms, the possible influence of amygdalectomy on such mechanisms is discussed.     

The Effects of Intra-amygdala Infusion of the AMPA Receptor Antagonist CNQX on Retention Performance Following Aversive Training

The aim of these experiments was to determine whether impaired retention performance in aversively motivated tasks, induced by blockade of amygdala AMPA receptors, is due to influences on mechanisms underlying memory retrieval or to other influences on performance. Rats received either footshock escape training (1 or 10 trials), or no foot shock, in a two-compartment straight alley and bilateral intra-amygdala infusions of the AMPA receptor antagonist CNQX (0.5 μg) were subsequently administered prior to inhibitory avoidance retention testing 8 days later. The CNQX impaired, but did not block, inhibitory avoidance retention performance as indicated by the initial latencies to enter the shock compartment. The animals were then retained in the alley until they remained in the starting compartment for 100 consecutive s and entries into the shock compartment were recorded as errors. In both the controls and CNQX-treated groups, increases in amount of original training resulted in fewer errors, indicating memory for the escape training. Furthermore, regardless of the amount of original training (i.e., 0, 1, or 10 trials), CNQX-treated groups made more errors. Other experiments examined intra-amygdala CNQX effects on reactivity to footshock, locomotor activity, and anxiety. CNQX decreased reactivity to footshock, blocked shock-induced decreases in locomotor activity, and had an anxiolytic effect in an elevated plus maze comparable to that induced by midazolam (0.5 μg). These findings suggest that intra-amygdala infusions of CNQX prior to retention testing affect inhibitory avoidance retention performance following aversive training by altering locomotor activity, reducing sensitivity to footshock, and reducing anxiety. The implications of these findings for hypotheses concerning amygdala function in aversively motivated learning and memory is discussed.     

What is both necessary and sufficient to maintain avoidance responding in the shuttle box?

To learn what maintains the frequency of shuttle box avoidance responses, male rats from the Berkeley S₁ strain, after 200 trials of standard discriminative avoidance training, were given 100 additional trials under one of four different conditions. Responding at the maximum rate was maintained when animals performed under the training conditions or when responses continued to terminate the warning signal immediately, even though shock was never given for failing to respond. In contrast, avoidance responding was reduced markedly if, and only if, trials were given in which the signal ceased to terminate immediately (i.e. it shut off either well before or well after a response). This decrement occurred even though avoidance responses continued to avert shock. Thus, under the conditions of this experiment prompt signal offset was both necessary and sufficient to maintain the occurrence of well-established shuttle box avoidance responses.     

Hormonal dissociation of limbic lesion effects on shuttle box avoidance in rats.

Rats with septal or hippocampal lesions, relative to normal rats, showed facilitated acquisition of a shuttle box avoidance response. The rats with septal lesions were also highly resistant to extinction compared with normal rats. When the same lesion effects were examined in hypophysectiomized rats, the animals with septal lesions continued to show facilitated performance, and those rats with hippocampal lesions performed no differently than nonoperated control animals. These findings are consistent with the hypothesis that the facilitated avoidance performance found in rats with hippocampal lesions is attributable to lesion-induced changes in hypophyseal activity, but similar changes induced by septal lesions are not.     

Running-wheel activity and avoidance in the mongolian gerbil

In the first of two experiments, running-wheel activity and unsignaled (Sidman) avoidance were studied in gerbils and albino rats. All gerbils ran at higher rates than any of the four rats studied. Under the avoidance procedure, four rats developed effective responding; the other two performed much less successfully. While avoidance developed more slowly in the gerbils, all showed asymptotic performance as effective as the four superior rats. The rats showed a consistent warm-up effect, receiving 60% to 80% of the total shocks in the initial third of the session. The gerbils displayed no warm-up, with shocks being evenly distributed over the session. Warm-up in the rats was not related to either response rate or to how effectively the animal was avoiding. When shock was removed, extinction occurred more rapidly in the rats than the gerbils. In the second experiment, which involved two-way shuttle avoidance, gerbils and albino mice quickly acquired the response. All animals met a criterion of 90% avoidance over 80 trials.     

Genetic differences in avoidance learning by Rattus norvegicus: escape/avoidance responding, sensitivity to electric shock, discrimination learning, and open-field behavior

The behaviors of rats selectively bred for either good or poor shuttle box avoidance learning were studied. The results of Experiment 1 indicated that the phenotypic difference in avoidance learning is not associated with differences in speed of escape or avoidance responding. Differences between the lines in frequency of intertrial responses (ITRs), which appear during training but not during pretest, suggest that ITRs in animals of the low-avoidance (SLA) line are more suppressed by electric shock than in animals of the high-avoidance (SHA) line. This result suggests that SLA animals may be more emotionally responsive than SHA animals. Experiment 2 demonstrated that the animals of the two lines do not differ in absolute sensitivity to electric shock, and Experiment 3 showed that the poor performance of the SLA line is not due to an inability to learn. Experiment 3 also provided evidence which suggests that the poor avoidance learning by SLA animals is due to their emotional reactivity. Observations of open-field behavior in Experiment 4 are consistent with this hypothesis. The major consistent correlate of the phenotypic difference in avoidance learning is greater emotionality or emotional reactivity in SLA than in SHA animals.     

Some behavioral effects of transecting ventral or dorsal fiber connections of the septum in the rat.

The behavioral effects of large electrolytic lesions in the septal area were compared with those of knife cuts that severed the ventral or dorsal connections of this structure. Rats with septal lesions lost weight and were transiently hyperdipsic. Ventral cuts produced similar effects, but dorsal cuts did not. All three operations decreased the latency to eat in a novel environment, increased the intake of sweetened milk, enhanced acquisition of a food-rewarded running response, and facilitated acquisition of a shuttle box avoidance response, The lesion, but neither of the knife cuts, reduced the effects of punishment and impaired the acquisition of a one-way avoidance response.     

Conditioned memory modulation, freezing, and avoidance as measures of amygdala-mediated conditioned fear

Three conditioned aversive responses were used to infer the existence of an unobservable central state of "conditioned fear," and the roles of certain amygdala subregions in producing these responses were investigated. Rats received tone-shock pairings in one compartment of a shuttle box and no tones or shocks in the other, distinctive, compartment. They were then trained to find food in one arm of a Y-maze. After the final training trial they were exposed to different sets of stimuli in the shuttle box with no shock. Twenty-four hours later rats that had received immediate posttraining exposure to the conditioned stimuli (in the shock-paired compartment) made significantly more correct responses on the Y-maze than rats that had been exposed to the neutral stimuli (in the no-shock compartment) or rats that had received delayed posttraining exposure to the conditioned stimuli. This constitutes a demonstration of posttraining memory modulation by conditioned aversive stimuli. Freezing increased during posttraining exposure to the conditioned stimuli compared to the neutral stimuli. When subsequently allowed to move freely between the two compartments, the rats in all groups also showed significant conditioned avoidance of the compartment containing the conditioned stimuli. In a second experiment the effects of lesions confined to specific parts of the amygdala on the three conditioned responses (memory modulation, freezing, avoidance) were tested. Lesions of the central nucleus impaired all three conditioned responses; lesions of the medial nucleus impaired conditioned modulation and avoidance. These lesions had no effect on freezing during the training trials. Lesions of the lateral and basolateral nuclei attenuated freezing during both training and testing. The findings suggest that the central and medial nuclei of the amygdala may be important parts of neural circuits mediating conditioned responses that constitute conditioned aversive states, but that conditioned freezing may be mediated independently.     

ACTH produces long-lasting recovery following partial extinction of an active avoidance response

Recent data suggest that ACTH administration produces recovery of an extinguished passive avoidance response at an unusually long injection-to-test interval. The present experiment sought to explore further the durability of recovery by examining the effect of ACTH following extinction of one-way active avoidance. Adult rats were injected with 16 IU ACTH, an equivalent volume of the ACTH vehicle gel, or saline 48 h after a previously learned active avoidance response was partially extinguished. Different groups from each treatment condition were tested 15 min, 24 h, or 7 days after injection. ACTH improved avoidance performance at all injection-to-test intervals relative to saline and vehicle gel injected controls. These data indicate that unlike reversal of other types of performance decrements, in which the effect of ACTH appears to be transient, administration of the hormone following an extinction treatment can produce enduring improvement of avoidance performance.