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 ability 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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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

Examined the effects of inescapable shock on subsequent escape performance and shock-elicited activity in 6 lines of mice (a total of 528 Ss in 6 experiments) 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-methylparatyrosine. 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. (18 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stress and adenosine: I. Effect of methylxanthine and amphetamine stimulants on learned helplessness in rats.

Examined, in 3 experiments involving 208 male albino rats, the effect of methylxanthine and amphetamine stimulants on deficits in shuttle-escape responding produced by earlier exposure to inescapable electric shock in rats. Caffeine completely reversed escape deficits in inescapably shocked rats when injected just before shuttle-escape testing but failed to prevent a test deficit when injected before shock pretreatment. Dose-response curves indicated that, whereas caffeine and theophylline were equally effective at reversing escape deficits, amphetamine not only failed to improve performance in preshocked rats but retarded escape in restrained (no-shock) controls. This amphetamine-induced deficit was reversed by co-treatment with caffeine. These data are discussed in terms of the role of adenosine receptor activation in helplessness and onservation–withdrawal. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Cross-stressor immunization against the behavioral deficits introduced by uncontrollable shock.

In 4 experiments with 204 male CD-1 mice, exposure to inescapable shock disrupted performance in both shock- (SE) and water-escape (WE) tasks. These deficits were prevented in Ss that were previously trained in the same task. However, an asymmetrical immunization effect was seen in a cross-stressor paradigm. Whereas deficits of WE performance engendered by inescapable shock were prevented by prior SE training, the deficits of SE were not eliminated by prior WE training. Evidently, the immunization effect occurs when initial training and subsequent testing are conducted in the same task or when the initial training and uncontrollable stress session involve the same aversive stimulus. Norepinephrine (NE) determinations revealed that reductions of NE introduced by inescapable shock were unaffected by prior SE training and were enhanced by prior exposure to the stress of water immersion. Thus, although the performance deficit introduced by inescapable shock may be related to variations of NE, the immunization effect probably was unrelated to alterations of NE. Data provisionally suggest that the immunization stems from 2 independent factors: Initially training Ss in an active escape task may (a) disrupt subsequent learning that the inescapable stress actually is uncontrollable and (b) limit the influence of the motor deficits introduced by uncontrollable shock on subsequent escape performance. (28 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Enhancing brain adenosine signaling with the nucleoside transport blocker NBTI (S-(4-nitrobenzyl)-6-theoinosine) mimics the effects of inescapable shock on later shuttle-escape performance in rats.

Experience with unsignaled, inescapable shock represents a profound challenge to brain metabolic function and physiology. The authors have argued that behavioral impairment following this traumatic stress is a consequence of enhanced brain adenosine signaling, which promotes metabolic recovery by profoundly inhibiting neural activation. The authors tested this hypothesis by artificially increasing extracellular brain adenosine concentration by blocking uptake transport with NBTI in rats given only restraint stress in five experiments. NBTI impaired shuttle-escape performance in the manner of inescapable shock in a dose-dependent manner and acted synergistically with an ineffective number of inescapable shocks to maximally impair test performance. These deficits produced by inescapable shock and NBTI were reversed by the nonselective adenosine receptor antagonist caffeine, and the highly selective A2A receptor antagonist CSC (8-(3-chloro-styrl)caffeine). The highly selective A? receptor antagonist DPCPX (8-Cyclopentyl-1,3-Dipropylxanthine) failed to improve performance in rats preexposed to inescapable shock or pretreated with NBTI. These data suggest that enhanced adenosine signaling at a brain A2A receptor impairs escape performance following inescapable shock in the learned helplessness paradigm. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Failure to learn to escape in rats previously exposed to inescapable shock depends on nature of escape response.

Results of previous studies show that dogs exposed to inescapable shocks in a Pavlov harness subsequently fail to learn to escape shock in a shuttle box. The present 6 experiments attempted to replicate this finding with male Sprague-Dawley rats (N = 182). In agreement with many previous investigations, Exp I found that Ss exposed to inescapable shock did not fail to learn to escape in a shuttle box. Exp II, III, and IV varied the number, intensity, and temporal interval between inescapable shocks and did not find failure to learn in the shuttle box. An analysis of responding in the shuttle box revealed that Ss shuttled rapidly from the very 1st trial, whereas dogs acquire shuttling more gradually. Exp V and VI revealed that Ss exposed to inescapable shock failed to learn to escape when the escape response was one that was acquired more gradually. Exp V utilized a double crossing of the shuttle box as the escape response and Exp VI utilized a wheel-turn response. (20 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Potentiation, overshadowing, and prior exposure to inescapable shock.

Four experiments are reported which explore the possibility that prior exposure to inescapable shock alters the way in which animals process information from responding during subsequent escape training. The stimulus consequences of responding were manipulated in each experiment. Rats received escapable shock, yoked, inescapable shock, or no shock prior to fixed ratio-2 (FR-2) shuttle escape training. A novel change in illumination following each shuttle response had opposite effects on inescapably shocked and control subjects. It dramatically improved the performance of inescapably shocked rats but impaired the performance of restrained subjects. The signal had no effect on escape trained animals. Response-produced auditory cues following each lever press on an FR-3 lever-press escape task were also observed to improve learning in inescapably shocked rats but to impair learning in restrained controls. The relation between lever pressing and the exteroceptive cue was manipulated. The exteroceptive cue enhanced learning in inescapably shocked rats when any two of the three required lever presses produced the cue. In contrast, the performance of restrained animals was impaired whenever the third response of the FR-3 produced the cue. Otherwise performance was unimpaired. The implications of these results are discussed with respect to the phenomena of potentiation and overshadowing, as well as to ways in which prior exposure to inescapable shock might alter information processing. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stress and adenosine: II. Adenosine analogs mimic the effect of inescapable shock on shuttle-escape performance in rats.

Examined, in 3 experiments involving 208 male rats, the role of adenosine regulation in escape deficits produced by earlier exposure to inescapable shock in rats (learned helplessness). Adenosine analogs injected before escape testing mimicked the effect of earlier inescapable shock, with the magnitude of the deficit varying with dose and drug specificity for A? adenosine receptors. Agonist-induced and stress-induced escape deficits were eliminated by pretest treatment with the centrally acting adenosine receptor antagonist theophylline but not the peripheral antagonist 8-[p-sulfophenyl]-theophylline. Finally, preexposure to an ineffective number of inescapable shocks interacted in synergy with an ineffective pretest injection of adenosine agonist to maximize deficits in escape performance. These data implicate energy regulation and a central compensatory action by adenosine in the aspects of helplessness related to onservation–withdrawal. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ventromedial septal lesions in rats reduce the effects of inescapable shock on escape performance and analgesia.

In 2 experiments with 104 male Sprague-Dawley rats, lesions of the ventromedial septum (VMS) reduced or eliminated several effects of exposure to inescapable shock, but lesions of the dorsolateral septum did not. Exp I demonstrated that VMS lesions reduced the loss in body weight produced by inescapable shock and eliminated the subsequent (24 hrs later) interference with escape performance (learned helplessness). Exp II demonstrated that VMS lesions reduced the analgesia that occurs immediately following inescapable shock and the analgesia reinstated by exposure to escapable shock 24 hrs later. Findings indicate that VMS lesions reduce several responses to inescapable shock and suggest the possibility that all of these effects may reflect a unitary deficit. It is hypothesized that VMS lesions reduce these effects of exposure to inescapable shock either by reducing the ability of the rats to learn that their responses and shocks were uncorrelated or by reducing the emotional impact of this lack of correlation. (52 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Catecholamine depletion in mice upon reexposure to stress: Mediation of the escape deficits produced by inescapable shock.

Reports 9 experiments with 372 male Swiss-Webster mice in which, immediately following exposure to 60 inescapable shocks, Ss had significantly reduced hypothalamic norepinephrine (NE). Within 24 hrs NE levels returned to control values. Reexposure to as few as 10 shocks 24 hrs after initial stress exposure resulted in significant decline of NE. At this interval after shock, escape performance was severely disrupted, with a large proportion of Ss exhibiting numerous failures to escape shock. Increasing brain dopamine (DA) and NE by levodopa treatment prior to shock prevented the escape deficits. Conversely, pairing 5 inescapable shocks with NE depletion by FLA-63, or both DA and NE depletion by alpha-methylparatyrosine, disrupted escape performance 24 hrs later. Residual drug effects, state dependence, or sustained amine turnover could not account for the behavioral changes. Data are discussed in terms of catecholamine mediation of escape performance through variations in response maintenance abilities. It is suggested that long-term effects of inescapable shock may be due to sensitization effects or conditioned amine depletion. (28 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Controllability and safety signals exert dissimilar proactive effects on nociception and escape performance.

In the present experiments we assess the ability of exteroceptive safety signals to proactively mimic shock controllability. In Experiment 1, animals were given escapable shock, yoked inescapable shock, restraint, or yoked shock with a stimulus coincident with shock offset on Day 1 and then given inescapable shock on Day 2. Safety signals attenuated the hypoalgesia following the first shock session. On Day 2, however, animals that had been preshocked with safety signals were not less hypoalgesic than those previously restrained. Conversely, shock controllability did not attenuate the hypoalgesia following the first session but proactively attenuated hypoalgesia during the second. Unlike animals preexposed to controllable shock, those given safety signals evidenced shuttle escape deficits 24 hr following the Day 2 inescapable shock treatment. Safety signals therefore failed to exert "immunization" effects. By employing identical preshock and shuttle test procedures, in Experiment 2 we demonstrated that safety signals completely block development of the escape deficit which otherwise results from the initial inescapable shock exposure. Thus, safety signals effectively reduce the impact of shock delivered in the same session but are ineffective in reducing the effect of subsequent shock. These results suggest that distinct processes underlie the effects of controllability and safety signals. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Failure to learn to escape by rats previously exposed to inescapable shock is partly produced by associative interference.

2 experiments demonstrated that the effects of prior exposure to inescapable shock on the subsequent acquisition of an escape response in rats is determined by the nature of the contingency that exists between responding and shock termination during the escape learning task, and not by the amount of effort required to make the response or the amount of shock that the S is forced to receive during each trial. Exp I, using 48 male Simonsen rats, showed that inescapably shocked Ss did not learn to escape shock in a shuttle box if 2 crossings of the shuttle box were required (fixed ratio, FR, -2) to terminate shock, but did learn this FR-2 response if a brief interruption of shock occurs after the 1st crossing of the FR-2. Exp II with 72 Ss showed that inescapably shocked Ss learned a single-crossing escape response as rapidly as did controls, but were severely retarded if a brief delay in shock termination was arranged to follow the response. Results are discussed in terms of the learned helplessness hypothesis, which assumes that prior exposure to inescapable shock results in associative interference. (15 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stressor-provoked behavioral changes in six strains of mice.

Behavioral changes induced by inescapable shock were examined in 6 strains of mice. Exposure to shock provoked time-dependent disturbances of shuttle escape performance. In some strains the shock treatment did not affect escape performance, whereas in others profound performance deficits were evident. The inescapable shock treatment induced strain-dependent alterations of performance in a forced-swim task. In most instances the shock treatment initially provoked invigorated responding, but in other strains the shock had no effect or depressed active responding. Y-maze spontaneous alteration performance was not affected by the shock treatment, although a strain-dependent increase of perseverative responses was evident. The occurrence of a stressor-induced deficit in 1 task in a particular strain was not predictive of behavioral alterations in a 2nd task. Data are discussed with respect to animal models of depression and genetic differences associated with response to stressors. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of task-irrelevant cues and reinforcement delay on choice-escape learning following inescapable shock: Evidence for a deficit in selective attention.

Five experiments with 152 male albino rats examined the conditions under which choice-escape learning in an automated Y-maze is impaired by pretreatment with inescapable shock. Ss exposed to inescapable shock made more errors and responded more slowly than did controls only when shock termination was delayed and task-irrelevant cues were present during choice-escape training. Findings are discussed in terms of information processing and neurochemical consequences of exposure to inescapable shock. It is suggested that the concurrent manipulation of irrelevant cues and reinforcement delay may have masked the choice contingency and increased task difficulty. Other possible explanations of the results include lessened attention to proprioceptive stimuli, differences in arousal levels between conditions, and depletion of norepinephrine in the locus coeruleus following inescapable shock. (35 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Helplessness and escape performance: Glutamate-adenosine interactions in the frontal cortex.

Adenosine has been implicated as a proximate mediator of escape deficits in the learned helplessness paradigm, suggesting that neuronal overactivation--a typical precursor to adenosine release--precedes the inescapable shock-induced impairment (T. R. Minor, W. C. Chang, & J. L. Winslow, 1994). In the present experiments, glutamate (100 μg) injection into the rat frontal cortex produced a deficit in escape performance. Pretest treatment with the adenosine receptor antagonist caffeine (7 mg/kg ip) reversed the effect of glutamate when infused 1 hr, but not 72 hr, after glutamate injection. Finally, microinjection of 2-amino-5-phosphonovaleric acid (5 ng) into the frontal cortex prior to inescapable shock prevented the escape deficit. These findings are consistent with the involvement of N-methyl-D-aspartate receptor activation in the frontal cortex in the helplessness effect. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Exposure to uncontrollable stress alters withdrawal from morphine.

Examined the influence of the controllability/uncontrollability of shock as a stressor on the severity of subsequent morphine withdrawal in 2 experiments with 84 male Holtzman rats. In Exp I (36 Ss), Ss that received 2 daily sessions of 80 yoked-inescapable shocks, in contrast to those given 80 escapable shocks or restrained without shock, showed an enhanced series of correlated withdrawal behaviors (i.e., mouthing, teeth chattering, head/body shakes) 24 hrs later when injected with morphine sulfate (5 mg/kg) followed by a naloxone HCl (5 mg/kg) challenge. In Exp II (48 Ss), this finding was replicated with escape-yoked-restrained Ss given saline injections during the pretreatment phase, but the impact that inescapable shock had on later precipitated withdrawal was completely blocked when Ss were administered naltrexone HCl (14 mg/kg) before each shock session. Findings are discussed in terms of the capability of inescapable shock to activate an endogenous opiate system, thereby leading to a sensitization of release or receptor processes that could protentiate later morphine withdrawal. (56 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Similarity between shock and safe areas during acquisition, transfer, and extinction of escape behavior in rats.

Demonstrated, in 3 experiments with a total of 128 female hooded rats, that performance in escape training was impaired when shock- and safe-box stimuli were similar rather than dissimilar to each other. Prior training with similar shock and safe boxes impaired responding during subsequent training or extinction under the dissimilar shock and safe condition. Prior training under the dissimilar condition did not reliably influence subsequent training or extinction under the similar shock-safe condition. Resistance to extinction under the dissimilar condition was reliably better following training with random presentations to both similar and dissimilar conditions than following training with the dissimilar condition alone. Exp III showed that impairment of escape behavior during training was attributable to response-contingent similarity between shock and safe boxes. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Dissociation of antinociception and escape deficits induced by stress in mice.

Six experiments (327 Swiss-Webster mice) assessed the conditions under which stress would induce antinociception in a subsequent hot-plate test. Both footshock and tail shock produced the antinociception. This effect was apparent with as little as a single shock trial. The magnitude of the antinociception was maximal following 15 shock presentations and was largely reduced after 60 shocks. In contrast to the results of R. L. Jackson et al (see record 1980-31880-001), whether stress was escapable was not a necessary feature needed to produce the antinociception. Moreover, the magnitude of the antinociception induced by stress was not enhanced in mice that had previously been exposed to stress. Finally, morphine (10.0, 20.0, and 30.0 mg/kg, ip) produced a pronounced antinociception but did not appreciably influence escape performance in a shuttle task in which performance was disrupted by inescapable shock. It is suggested that the antinociception and shuttle-escape deficits induced by uncontrollable shock are independent of one another. (27 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Learned helplessness and immunization: Sensitivity to response–reinforcer independence in immunized rats.

Exps I and II, with 62 male Holtzman rats, examined the learned helplessness and immunization effects using a test in which appetitive responding was extinguished by delivering noncontingent reinforcers. Contrary to learned helplessness theory, "immunized" Ss showed performance virtually identical to that of Ss exposed only to inescapable shock and different from that of nonshock controls. Exp II suggested that the helplessness effect and the lack of immunization were not due to direct response suppression resulting from shock. In Exp III, in which the immunization effect was assessed in 28 Ss by measuring the acquisition of a response to obtain food when there was a positive response–reinforcer contingency, immunization was observed. Results cannot be explained on the basis of proactive interference and instead suggest that Ss exposed to the immunization procedure acquired an expectancy of response–reinforcer independence during inescapable shock. Thus, immunization effects may reflect the differential expression of expectancies rather than their differential acquisition as learned helplessness theory postulates. (55 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)