The time course of learned helplessness, inactivity, and nociceptive deficits in rats

Four experiments are reported which explore the nature of the effects of inescapable shock on subsequent shuttlebox escape learning. The first experiment demonstrated that shuttle escape deficits dissipate within 48 hr after treatment with inescapable shock. Experiment 2 showed that exposure to inescapable shock suppressed unlearned activity in the shuttlebox and that this activity deficit recovered within 48 hr. Experiment 2A demonstrated that this shuttlebox crossing decrement was at least partly attributable to the inescapability of the shocks. These results suggested that activity factors might partly mediate the shuttle escape learning deficit reported in Experiment 1. Experiment 3 explored the possibility that activity and shuttle escape learning deficits are subserved by the effects of inescapable shock on pain sensitivity. The results supported this notion. It was found that rats were less sensitive to painful stimulation 24 hr after inescapable shock and that this analgesic tendency also dissipated within 48 hr after pretreatment. The implications of these results were discussed.     

Learned helplessness in the rat: time course, immunization, and reversibility.

Rats, like dogs, fail to escape following exposure to inescapable shock. This failure to escape does not dissipate in time; rats fail to escape 5 min, 1 hr., 4 hr., 24 hr., and 1 wk. after receiving inescapable shock. Rats that first learned to jump up to escape were not retarded later at bar pressing to escape following inescapable shock. Failure to escape can be broken up by forcibly exposing the rat to an escape contingency. Therefore, the effects of inescapable shock in the rat parallel learned helplessness effects in the dog.     

Escape performance after inescapable shock in selectively bred lines of mice: response maintenance and catecholamine activity.

The effects of inescapable shock on subsequent escape performance and shock-elicited activity were examined in six lines of mice selectively bred for differences in general locomotor activity. The line differences in locomotor activity were found to be unrelated to the differences observed on shock-elicited activity. However, escape performance following exposure to inescapable shock was predictable from the levels of shock-elicited activity. Those lines that displayed the greatest decline in motor activity during shock likewise displayed the most pronounced escape deficits. The line differences in escape performance induced by inescapable shock could be mimicked by treatment with a tyrosine hydroxylase inhibitor, alpha-methyl-p-tyrosine. As predicted, the lines that displayed the least interference after tyrosine hydroxylase inhibition exhibited the smallest reduction in levels of catecholamines. The effects on escape performance following inescapable shock are interpreted in terms of the role of response maintenance deficits produced by catecholamine depletion.     

The role of norepinephrine and acetylcholine in mediating escape deficits produced by inescapable shocks

This study examined the role of neurochemical changes produced by inescapable shock, specifically the depletion of norepinephrine (NE) and enhancement of acetylcholine (ACh), in mediating subsequent inescapable shock-induced deficits in escape acquisition in rats. Enhancement of these neurochemical changes by injections of the NE synthesis inhibitor, FLA-63 (10 mg/kg), or the anticholinesterase, eserine sulphate (3 X 0.5 mg/kg), during the inescapable shock enhanced the subsequent escape deficits observed 3 days later. In contrast, these drugs had no effect on the subsequent escape behavior of rats that were not exposed to inescapable shock. Since these effects could not be attributed to carry-over or state-dependent effects of the drugs, these data suggest that the magnitude of the escape deficit produced by prior inescapable shock is dependent on the magnitude of the initial inescapable shock-induced changes in NE and ACh.     

Prior exposure to inescapable electric shock in rats affects extinction behavior after the successful acquisition of an escape response

In Expt 1, rats exposed to 64 inescapable electric shocks in a restrainer or merely restrained were later given either 0, 5, 15 or 30 escape/avoidance training trials with a two-way shuttlebox procedure that does not lead to interference with escape acquisition due to prior exposure to inescapable shock. After escape training all rats were given an escape/avoidance extinction procedure in which shock was inescapable. The rats which had received prior exposure to inescapable shock responded less often and with longer latencies in extinction than did the restrained rats. Experiment 2 demonstrated that this effect is caused by the inescapability of the initial shock treatment. These results were explained in terms of (a) associative interference which minimized the effect of shuttlebox escape training for the preshocked subjects, and (b) a stronger tendency to recognize the presence of an inescapable shock situation during extinction for the preshocked subjects. The relationship between these results and previous work demonstrating that exposure to the escape contingency mitigates the effects of inescapable shock exposure was also discussed.     

Acute and chronic stress effects on performance in a forced-swim task

The effects of uncontrollable stressors on performance in a subsequent forced-swim paradigm were assessed in mice. Uncontrollable shock initially induced behavioral invigoration; however, within 24 h of stressor application, swimming behavior was depressed relative to nonstressed mice. The controllability of the stressor did not influence the initial invigoration, being present among escapably shocked mice as well as among mice that received (yoked) inescapable shock. In contrast, the depression of responding evident 24 h after stressor application was related to the availability of behavioral coping methods. Finally, following repeated exposure to footshock there was no indication of adaptation to the behavioral changes ordinarily induced by acute shock stress. The data were related to the effects of uncontrollable stressors on escape performance, and with respect to the use of this preparation as an animal model of human depression.     

Immunization of opioid analgesia: Effects of prior escapable shock on subsequent shock-induced and morphine-induced antinociception

In Experiment 1, it was shown that experience with escapable foot shock 4 hr prior to a session of 80 inescapable tail shocks prevented the occurrence of an analgesic response normally observed immediately following the tail shock. It has been suggested by J. W. Grau, R. L. Hyson, S. F. Maier, J. Madden, and J. D. Barchas (Science, 1981, 213, 1409–1411) that the analgesia that occurs following this number of inescapable tail shocks is mediated by endogenous opioid systems. To further explore the influence of escapable shock on opiate-mediated analgesia, Experiment 2 examined the effects of prior escapable shock on the long-term analgesia reaction that occurs upon brief exposure to shock 20 hr after morphine administration. Rats were given escapable shock, inescapable shock, or no shock 4 hr prior to a morphine injection. Twenty hours following the injection, all subjects received 5 brief foot shocks and were then immediately given tail-flick analgesia tests. Subjects which received inescapable shock or no shock prior to the morphine injection displayed a significant analgesic response. However, subjects which received escapable shock prior to morphine were not analgesic following brief exposure to shock. Thus, escapable shock seems to directly influence the activation of opioid analgesia systems.     

The effects of escape conditioning and shock intensity on responding during inescapable shock

Eight albino rats, conditioned to press a lever to escape shock, continued to lever press during short inescapable shocks presented subsequently. The rate of this behavior was found to be higher for higher shock intensities regardless of the order in which shock values were presented. Relative to the immediately preceding escape rate, responding during inescapable shock was higher following conditioning at higher fixed-ratio escape requirements. Four subjects not conditioned to escape shock pressed the lever very infrequently during inescapable shock and showed little change with changes in shock intensity. The escape conditioning effects suggest that responding during inescapable shock is superstitious escape behavior. The effects of shock intensity on this behavior appear to be similar to reported effects of shock intensity on escape behavior.     

Effects of signaling inescapable shock on subsequent escape learning: implications for theories of coping and "learned helplessness"

The present experiments reveal that shuttle-escape performance deficits are eliminated when exteroceptive cues are paired with inescapable shock. Experiment 1 indicated that, as in instrumental control, a signal following inescapable shock eliminated later escape performance deficits. Subsequent experiments revealed that both forward and backward pairings between signals and inescapable shock attenuated performance deficits. However, the data also suggest that the impact of these temporal relations may be modulated by qualitative aspects of the cues because the effects of these relations depended upon whether an increase or decrease in illumination (Experiment 2) or a compound auditory cue (Experiment 4) was used. Preliminary evidence suggests that the ability of illumination cues to block escape learning deficits may be related to their to reduce contextual fear (Experiment 3). The implications of these data for conceptions of instrumental control and the role of fear in the etiology of effects of inescapable shock exposure are discussed.     

Therapy and immunization of long-term analgesia in rats

Three experiments are reported which examine the effects of experience with escapable shock either subsequent to (Experiment 1) or prior to (Experiments 2 and 3) a session of inescapable shock on the subsequently produced long-term analgesic reaction in rats. Experment 1 demonstrated that experience with escapable shock 4 hr after a session of inescapable tail shock completely reverses the analgesic response that is normally observed 24 hr later upon reexposure to shock. The escapability of the shock was shown to be the important factor in reversing the analgesic reaction, since subjects given inescapable shock in amounts equivalent to escape subjects exhibited no reduction in analgesia. Experiment 2 showed that experience with escapable shock 4 hr prior to a session of inescapable tail shock could also completely eliminate the long-term analgesic reaction. Experiment 3 replicated the results of Experiment 2, but employed a different escape task and temporal parameters in order to extend the generality of the findings, and to more closely match the procedures employed in behavioral experiments reported by J. L. Williams and S. F. Maier (Journal of Experimental Psychology: Animal Behavior Processes, 1977, 3, 240–253). The implications of these results for the areas of pain control and learned helplessness were discussed.     

Exposure to inescapable shock produces both activity and associative deficits in the rat

Interference with shuttle-box escape learning following exposure to inescapable shock is often difficult to obtain in rats. The first experiment investigated the role of shock intensity during escape training in the apparent fragility of the effect. Experiment 1A demonstrated that the magnitude of the interference effect was systematically related to shock intensity during shuttle-box testing. At .6 mA, a robust effect was obtained, whereas at .8 mA and 1.0, little or no deficit in the escape performance of inescapably shocked rats was observed. Experiment 1B demonstrated that the deficit observed in Experiment 1A depended upon whether or not rats could control shock offset. Experiment 2 suggested that preshock may suppress activity and that higher shock levels may overcome this deficit. Experiment 3 tested this as the sole cause of the escape deficit by requiring an escape response which exceeded the level of activity readily elicited by a 1.0-mA shock in both restrained and preshocked rats. In such a task, preshocked rats performed more poorly than did restrained controls. These results are consistent with the possibility that inescapable shock may, in addition to reducing activity, produce an associative deficit. Experiment 4 more clearly demonstrated that inescapable shock produces deficits in performance which cannot be expleined by activity deficits and which appear to be associative in nature. It was shown that inescapable shock interfered with the acquisition of signaled punishment suppression but not CER suppression. The theoretical implications of these data for explanations of the manner in which prior exposure to inescapable shock interferes with escape learning were discussed.     

Experimental self-punishment and superstitious escape behavior

Rats were trained to escape from shock by pressing a bar. Bar holding was subsequently punished with very brief shocks. This treatment failed to depress bar-holding behavior. In some cases, although the escape shocks were delivered very infrequently, bar holding was maintained and resulted in the delivery of several thousand punishments per session. These and other effects of the punishment treatment were investigated. Finally, some of the possibilities of superstitious escape responding were explored by presenting inescapable shocks to rats that had been trained to escape shock by lever pressing. Although responding during these shocks had no programmed consequences, responding was sustained.     

Opiate antagonists and long-term analgesic reaction induced by inescapable shock in rats

Five experiments examined the influence of opiate antagonists on both the short-term analgesic reaction resulting 30 min after exposure to inescapable shock and the long-term analgesic reaction resulting after reexposure to shock 24 hr after inescapable shock exposure. Experiment 1 showed that the long-term analgesic reaction could be reduced by administration of naltrexone prior to exposure to inescapable tail shock. Experiment 2 showed that the reduction in the long-term analgesic reaction produced by naltrexone was dose-dependent. Experiment 3 showed that the long-term analgesic reaction could also be reduced by administration of naltrexone prior to reexposure to shock. Experiment 4 showed that the long-term analgesic reaction could be reduced by administration of large dose of naloxone prior to reexposure to shock. Experiment 5 showed that the short-term analgesic reaction was reduced by naltrexone administered prior to inescapable shock. Some implications of these results for the biochemical substrates of both learned helplessness and stress-induced analgesia are discussed.     

Modeling signal features of escape response: effects of cessation conditioning in "learned helplessness" paradigm

Six experiments examined the effects of signaling the termination of inescapable shock (cessation conditioning) or shock-free periods (backward conditioning) on later escape deficits in the learned helplessness paradigm, using rats (Sprague-Dawley and Bantin-Kingman). A cessation signal prevented later performance deficits when highly variable inescapable shock durations were used during pretreatment. The inclusion of short minimum intertrial intervals during pretreatment did not alter the benefits of cessation conditioning but eliminated the protection afforded by a safety signal. The beneficial effects of both cessation and backward signals were eliminated when a single stimulus signaled shock termination and a shock-free period. Finally, a combination of cessation and backward signals was found to be most effective in immunizing against the effects of subsequent unsignaled, inescapable shock on later escape performance. These data suggest that cessation conditioning may be crucial to the prophylactic action of an escape response.     

Inescapable shock and attention to internal versus external cues in a water discrimination escape task

In these experiments we examined discrimination learning in a water escape task following exposure to escapable, yoked inescapable, or no electric shock. Inescapable shock did not have an effect on swim speeds in any of the experiments. Inescapable shock interfered with the acquisition of a position (left-right) discrimination when an irrelevant brightness cue (black and white stimuli) was present. However, inescapable shock did not affect the acquisition of the position discrimination when the irrelevant brightness cue was removed. Inescapably shocked subjects showed facilitated learning relative to escapably shocked and nonshocked subjects when the brightness cue was included as a relevant cue. These data may resolve discrepancies between studies that did, and did not, find inescapable shock to interfere with the acquisition of discriminations. Moreover, they point to attentional processes as one locus of the cognitive changes produced by inescapable shock and suggest that exposure to inescapable shock biases attention away from "internal" response-related cues toward "external" cues.     

Emotionality in selectively bred strains of rats mediates prior shock effects on escape-avoidance conditioning.

Rats of the Maudsley Reactive and Maudsley Non-reactive strains were given 25 trials of escape-avoidance conditioning after exposure to inescapable shock. Prior shock exposure (PSE) did not affect avoidance or escape latencies, but decreased the number of avoidances made by the Maudsley non-reactive animals and increased the number of their failures to escape. The results are interpreted as demonstrating an interference with the classical conditioning of a conditioned emotional response, through a reduction in the information content of the CS following PSE. The strain differences are interpreted as due to the non-reactive animals being especially sensitive to PSE.     

The generality of learned helplessness in the rat

Two experiments were simultaneously conducted in which two different groups of 40 rats each were exposed to one of two different stressors. In both experiments half the subjects were pretreated with shock, half with underwater exposure. For each pretreatment stressor, half the subjects were allowed to escape, the other half were not. The experiments differed in the test task used. Approximately 24 hr after pretreatment, one-half the subjects from each pretreatment group received 20 water-escape trials in an underwater maze, the other half received 20 shock-escape trials in a two-way shuttle box. The subjects in each of the inescapable pretreatment conditions were slower to escape in the subsequent shock-escape and water-escape tasks when compared with subjects in the corresponding escapable pretreatment condition. The “learned helplessness” effect appeared to be no smaller when aversive stimuli were changed between pretreatment and test than when they remained the same.     

Learned helplessness in the rat.

Four experiments attempted to produce behavior in the rat parallel to the behavior characteristic of learned helplessness in the dog. When rats received escapable, inescapable, or no shock and were later tested in jump-up escape, both inescapable and no-shock controls failed to escape. When bar pressing, rather than jumping up, was used as the tested escape response, fixed ratio (FR) 3 was interfered with by inescapable shock, but not lesser ratios. With FR-3, the no-shock control escaped well. Interference with escape was shown to be a function of the inescapability of shock and not shock per se: Rats that were "put through" and learned a prior jump-up escape did not become passive, but their yoked, inescapable partners did. Rats, as well as dogs, fail to escape shock as a function of prior inescapability, exhibiting learned helplessness.     

Forced exercise blocks learned helplessness in the cockroach (Periplaneta americana)

For three consecutive days, two groups of adult female cockroaches (Periplaneta americana) (ns = 10) received inescapable shock. 24 hr. later one group was exposed to 10 min. of forced exercise on a treadmill while the other group received no exercise. Both groups were then run in a shuttlebox escape task. The cockroaches exposed to forced exercise did not become helpless in the shuttlebox escape task.