Ethological analysis of predator avoidance by the paradise fish (Macropodus opercularis L.): II. Key stimuli in avoidance learning

The possible role of eyespot patterns in predator recognition by paradise fish was examined using a passive avoidance conditioning technique with various dummies or live goldfish. It was found that a low-intensity shock, although clearly uncomfortable, elicited exploratory behavior in the fish and that observable learning did not occur. However, if the paradise fish was shocked in the presence of a live goldfish or various fish dummies, exploration diminished and avoidance learning was detected. This was characterized by a considerable increase in latency to enter the shocked compartment. The most effective dummies were those with two laterally arranged eye-like spots. The possible role of species-specific key stimuli in avoidance learning and organizing defensive behavior of the paradise fish is discussed.     

Generality of the failure-to-escape (helplessness) phenomenon in rats

A series of four experiments investigated a number of parameters reported to produce “helplessness” in rats. Consistent differences in escape behavior were not found between inescapably shocked and restrained rats when a FR 1 shuttling response was used. Escape latencies also did not differ between groups when a reduced shock intensity was employed during escape training in FR 2 procedure or when an increased FR 3 response was employed during escape training. Findings are discussed in terms of the robustness of the failure-to-escape phenomenon from which “helplessness” in the rat is inferred.     

Reinstatement of fear to an extinguished conditioned context

Rats were shocked in the black but not the white compartment of a shuttlebox and then exposed to the black compartment in the absence of the shock unconditioned stimulus (US) to extinguish fear responses (passive avoidance). In five experiments, rats were then shocked in a reinstatement context (distinctively different from the shuttlebox) to determine the conditions that reinstate extinguished fear responding to the black compartment. Rats shocked immediately upon exposure to the reinstatement chamber failed to show either reinstatement of avoidance of the black compartment or fear responses (freezing) when tested in the reinstatement chamber. In contrast, rats shocked 30 sec after exposure to the reinstatement chamber exhibited both reinstatement of avoidance of the black compartment and freezing responses in the reinstatement chamber (Experiment 1). Rats shocked after 30 sec of exposure to the reinstatement chamber but then exposed to that chamber in the absence of shock failed to exhibit reinstatement of the avoidance response and did not freeze when tested in the reinstatement chamber (Experiment 2). Rats exposed to a signaled shock in the reinstatement chamber and then exposed to that chamber in the absence of shock also failed to exhibit reinstatement of the avoidance response (Experiment 5). These rats showed fear responses to the signal but not to the reinstatement chamber. Finally, rats exposed for some time (20 min) to the reinstatement chamber before shock exhibited reinstatement of the avoidance response but failed to freeze when tested in the reinstatement chamber (Experiments 3 and 4). These results are discussed in terms of the contextual conditioning (Bouton, 1994) and the US representation (Rescorla, 1979) accounts of postextinction reinstatement.     

Classical conditioning of an “avoidance” response in goldfish using a linear presentation procedure

The present study examined the nature of the “avoidance” response in goldfish under the linear presentation procedure (Zerbolio, 1981). With this procedure, shuttling behavior occurring during the presentation of the trial stimulus produces either CS? or CS+, and further occurrence of shuttling within the trial interval (10 sec) changes the value of CS from negative to positive, or vice versa. If the fish remains in the compartment when the prevailing cue state is CS? at the end of the interval, shock can be avoided. With this procedure fish responded to the CS+ more than to the CS? and avoided shock. But fish in one of two control groups, in which responses had no effect in changing the cue state from CS+ to CS?, or vice versa, also showed a clear differentiation. The results were generally in line with the view that the “avoidance” response in fish is acquired through classical conditioning. The contribution of classical conditioning to the acquisition of avoidance response is discussed.     

Conditions of preexposure and passive avoidance behavior in rats

In the first experiment, rats given a 5-min period of preexposure (simple exploration) to a two-compartment box showed poorer passive avoidance of the compartment where they were subsequently shocked than a control group which was not preexposed to the apparatus. The second experiment involved preexposure to sugared milk (SM), flashing light and loud noise (LN), or simply the apparatus (EC). One group received no exposure to the apparatus (NC). Following one shock trial, the groups were ordered LN > NC > EC > SM from most to least passive avoidance. The results were discussed in the context of latent inhibition and an averaging model of positive and negative events.     

Contextual associations in trace conditioning

Rats were given tone-footshock pairings with a 0-, 10-, or 30-sec trace interval between tone offset and shock onset. Half the rats within each trace interval were tested for their conditioned fear of the tone through a lick suppression procedure; the remaining rats were evaluated for their fear of the background or contextual cues through their avoidance of the compartment in which conditioning had occurred. Less conditioning was observed to the tone with increasing trace intervals. However, conditioned fear of the context increased with increases in the trace duration. The ability of the more predictive stimulus, the tone, to overshadow the contextual cues was determined by the tone’s temporal contiguity with the footshock. The need to incorporate temporal parameters within current theories of conditioning is discussed.     

The effect of number and minimum duration of post-response-prevention escapes on the resistance to extinction of an avoidance response

After one-way avoidance training, rats were exposed, during avoidance response prevention, to light (CS-only) presentations or to light-shock (CS-US) pairings. Subgroups were then given 1, 5, or 10 trials during which they could escape immediately (unrestricted) or after 5 sec (restricted) by means of the previously conditioned avoidance response from a simultaneous light-shock compound. All animals were then exposed to avoidance extinction. The number of unrestricted escapes increased responding for CS-only animals, but had no significant effect on the performance of CS-US animals. Nevertheless, resistance to extinction was considerably less for CS-only animals given 10 unrestricted escapes than for CS-US animals given one unrestricted escape. One restricted escape had no more effect than one unrestricted escape for either response-prevention group. However, 5 restricted escapes elevated responding for CS-only animals to the level of CS-US animals. Extinction responding for CS-US animals increased significantly only after 10 restricted escapes. Since CS-only animals showed no further increase, resistance to extinction once more was greater for CS-US animals. These results, together with the very brief unrestricted escape latencies of CS-only animals, support a greater role for Pavlovian extinction than for response competition in the facilitation of avoidance extinction by CS-only response prevention. The fact that 10 restricted escapes were required to elevate resistance to extinction for CS-US animals over that obtained with one unrestricted escape attests to the effectiveness of Pavlovian conditioning during avoidance response prevention in elevating CS aversiveness to a near ceiling level.     

Conditions that potentiate the effects of electroconvulsive shock administered 24 hours after avoidance training

Three experiments assessed the conditions that potentiate effects of an electroconvulsive shock (ECS) administered 24 h after avoidance training. Stimuli present immediately prior to the ECS were systematically varied. In Experiment 1, which employed a passive avoidance task, the primary determinant of whether the ECS disrupted retention was whether the situational cues present at the time of ECS delivery were those associated with the initial training experience: ECS disrupted performance only when it was administered in the original training apparatus, regardless of whether or not a footshock was presented immediately prior to ECS. In Experiment 2, which employed an active, shuttlebox avoidance task, both the situational cues from the training apparatus and a footshock were necessary to potentiate the disruptive effects of the ECS. Experiment 3 revealed that ECS effects on performance of the active avoidance task can also be potentiated by a combination of apparatus cues and the warning signal used in initial training. These results are interpreted as indicating that informational functions of stimuli present when an ECS is administered are important determinants of the effects of the ECS.     

Defensive burying in rats and hamsters

Hooded rats and golden hamsters were shocked by one of two prods in a chamber with a sawdust-covered floor. Rats buried the prod through which they had been shocked, but hamsters displayed no burying behavior. Hamsters may not have buried the prod because they could not perform the required motor pattern. However, hamsters can carry and pile food pellets. Therefore, in a second experiment, rats and hamsters were shocked in a chamber with wooden blocks on the floor. Rats piled blocks around the prod through which they had been shocked, but hamsters did not. The third experiment established that, like rats, hamsters can associate a prod with shock in one trial, since they showed differential avoidance of a prod through which they had been shocked. Since hamsters are nonsocial and rats are social, these results are consistent with suggestions that burying sources of aversive stimulation evolved as an altruistic behavior.     

Defensive burying in the rat: A behavioral field analysis

Time spent in various behaviors by the rat was recorded in a defensive burying paradigm. Experiment 1 revealed that rats spent more time burying the shock prod than a control prod and that doubling the size of the test chamber did not have a significant effect on the time spent in any behavior. In Experiment 2, the location of bedding material in a two-compartment test chamber was found to affect the occurrence of burying (both the shock and control prods) and burrowing behavior. Burying did not occur when bedding was not available in the shock compartment but was located in the escape compartment. Burrowing was more likely to occur when bedding was in both compartments than when it was in only one compartment. Immobility and escape latencies were shorter than burying latencies in all subjects. Burying was viewed as belonging to a second stage of defensive behavior.     

Instrumental electrodermal conditioning in the monkey (Cebus albifrons): Acquisition and long-term retention

EightCebus albifrons monkeys received 25 sessions of discriminative operant conditioning of the skin conductance response (SCR), with colored lights as discriminative stimuli and with Sidman avoidance (SS-40 sec, RS-40 sec) scheduled during one light and response-contingent shock during the other, Discriminative stimulus segments were separated by 30-sec periods of time-out from shocks and lights, Two extinction sessions were run 3 months after training, Almost from the beginning of conditioning, the monkeys made significantly more unelicited skin conductance responses in the avoidance periods than in punishment, The monkeys’ heart rates also increased significantly, but there was no difference between avoidance and punishment, SCR frequency during extinction continued to differentiate significantly between avoidance and punishment, and there was a significant increase in this differentiation from the last conditioning session to the first extinction session, but the difference then reduced in the second session, The results indicated that monkey’s SCRs are influenced by instrumental reinforcement contingencies somewhat in the same fashion as those of humans.     

Effects of the correlation between a positive and negative US on conditioned suppression in rats

For three groups of rats, an auditory CS, presented while the animals were responding on a variable-interval schedule for food reinforcement, was terminated on half of the trials with a noncontingent footshock. For two groups, half of the trials were also followed after 5 sec by the delivery of free food. In the positively correlated condition (PC) the free food was presented on shocked trials and in the negatively correlated condition (NC) on the nonshocked trials, while the remaining group (S) never received free food. In a fourth group the shock was omitted and free food delivered on half of the trials. Although all shocked groups showed a significant suppression, the magnitude was greater for Group PC than for Groups NC and S, which did not differ. Suppression did not result from the pairing of the CS with food alone. These results do not support the counterconditioning hypothesis that the pairing of a normally noxious stimulus with food reduces its aversiveness.     

The effect of controllable and uncontrollable neonatal preshocks on adult escape/avoidance behavior in the guinea pig (Cavia porcellus)

Neonatal guinea pigs were given escapable, inescapable, or no shock and were later tested as adults on a signaled escape/avoidance task. During the neonatal period, the animals that could escape shock learned to do so quickly and steadily increased their overall level of activity, while those that could not, displayed a consistent decline in activity. Furthermore, during adult escape/avoidance sessions, guinea pigs, that could control neonatal shock were superior to those that lacked such control. These findings extend the generality of the interference effect to the guinea pig and highlight the influence of early control of aversive events on this phenomenon.     

Long-term retention of fear-potentiated startle following a short training session

The permanence of aversive memories has been reported to vary when assessed with conditioned emotional response procedures (months) versus avoidance response measures (days). When evaluated with the potentiated startle paradigm, five light-shock pairings at a 2-min intertrial interval produced highly reliable potentiated startle, which was similar in magnitude from 1 to 28 days after training and maximal using a 0.6-mA footshock intensity. These results are consistent with such measures as conditioned emotional response procedures, in which aversive memories have been observed after months following originaltraining. The results obtained with various shock intensities are also discussed in the context of other indices of fear.     

Footshock-produced excitation and inhibition of activity in rats

Hooded rats received five 1-sec shock presentations of 0.3, 0.5, or 1.0 mA. Activity measures recorded during each 30-sec intershock interval and at various retention intervals (.10, 2.5, and 24 h) following footshock (FS) indicated that (a) 5 sec after FS activity is directly related to shock intensity, while 10–30 sec following FS activity is inversely related to shock intensity; (b) the rate of decline in activity following FS increases with successive shock presentations; (c) activity is greater 10 h after FS than at a 2.5- or 24-h retention interval; and finally (d) shock compartment confinement increased activity and resulted in a substantial alteration in the form of retention curve in the 0.3-mA group but had lesser effects upon the retention curves of the 0.5- and 1.0-mA groups. The data were interpreted as supporting the hypothesis that the “incubation effect” is a result of a decline of the activating effects of FS.     

Effects of acute shock on body weight are mediated by changes in food intake

We examined the causal role of decreased food intake in the body weight pattern observed after exposure to intermittent footshock. In Experiment 1, relative to controls, shocked animals decreased food intake and lost weight in the 24-h test. An unshocked group whose food intake was yoked to the shocked group (food-yoked group) for the poststress period revealed that food intake was a sufficient cause of the body weight loss. In Experiment 2, after the first 24 h, the shock group recovered food intake and body weight gain but did not compensate for the initial losses. Body weights of food-yoked animals again indicated that food intake was a sufficient cause of these effects. The lowered body weight of shocked animals at the end of testing was due to a transient hypoingestion and a failure to subsequently show a compensatory hyperingestion. Dess’s (1991) regulatory shift hypothesis is refined in the light of these findings.     

Multiple deficits in the retention of an appetitively motivated behavior across a 24-h period in rats

Recent investigations have found a multiphasic retention function associated with avoidance training (e.g., Holloway & Wansley, 1973a, b). The present experiment was done to determine if a similar retention function also describes appetitively motivated behavior. Rats were allowed access to preferred solution in the shock compartment of a passive avoidance apparatus. Then either .25 h after the appetitive preexposure or at successive 3-h intervals up to 24 h, the rats were administered one-trial passive avoidance training consisting of a strong shock presented in the shock compartment. The retention of the appetitive preexposure was determined by its effect on performance of the passive avoidance task as measured 24 h after the shock trial. The results demonstrated that the retention function associated with the appetitive preexposure was phasic with an alternation between high and low retention every 12 h. Specifically, retention was higher after the .25-, 9-, 12-, and 24-h intervals than after 3-, 6-, 15-, and 18-h intervals. These results are consistent with prior research on the retention of avoidance training.     

Dissimilarity of mechanisms for evocation of escape and avoidance responding in dogs

Two groups of dogs were compared on the ability of an aversive Pavlovian CS to evoke a negatively reinforced instrumental response. For one group, the instrumental training was avoidance; for the other, escape. When presented alone, the CS evoked the instrumental response only from the avoidance group. Failure of the CS to evoke the response from the escape group poses difficulties for theories which characterize the initiation of avoidance responses as “escapes” from CS.     

Conditioned aversion is promoted by memory of CS−

Five experiments tested the effects of experience with a white compartment not paired with footshock (CS?) on conditioning of an aversion to a black compartment paired with footshock. As previously found with odors as CSs, a single pairing of the CS+ with footshock yielded significant conditioning only if the animal was also exposed to CS?, with greater conditioning when the CS? exposure preceded the CS+ than when the CS+ preceded the CS?. If, however, the CS? preceded CS+ by a 24-h interval, it was ineffective and no CS+ conditioning occurred. For adult rats, the effectiveness of the CS?/CS+ “integration” progressively decreased with increasing length of the interval separating their occurrence, although it was still significant (i.e., some CS+ conditioning occurred) with a 12-h CS? to CS+ delay. For preweanlings (16 days postnatal), no conditioning to CS+ occurred if the interval between CS? and CS+ was 1 h or longer, although significant conditioning to CS+ did occur with a CS? to CS+ interval as long as 40 min. It was as if active memory for the CS? at the time of CS+ exposure was necessary for CS+ conditioning, and forgetting of the CS? memory proceeded more rapidly for preweanling than for adult rats. Collectively, these experiments extend results previously indicating that (1) the CS+ contiguous to the US may or may not be “selected” for conditioning, depending on the rat’s exposure to, or memory for, a CS?, and (2) this stimulus selection might differ for immature and mature rats.     

The role of predictability in preventing escape deficits following loss of control over food acquisition

The present experiment examined whether predictability of food acquisition would eliminate the impairment of subsequent escape performance that otherwise resulted from uncontrollability over food acquisition. In pretreatment, the yoked and the yoked-signal groups received response-independent food at the same times as the experimental group acquired it on an FR 5/20 lever-press schedule. However, a pellet presented for the yoked-signal group followed a 1.5-sqc tone, which served as a predictive signal of food. The naive control group received the same clumber of pellets in their home cages in this phase. Results of the escape latency in the subsequent FR 2 shuttling shock-escape test indicated that the predictability of outcome eliminated the escape deficits showed by the yoked-non signal group. This modulating effect of a predictive signal is hypothesized to be due to an overshadowing of uncontrollability by predictability.