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.     

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.     

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.     

Shock signals and the development of stress-induced analgesia

We report five experiments in which we investigated the effects of "feedback signals" on the pattern of hypoalgesia produced by inescapable shocks. A 5-s lights-out stimulus coincident with shock termination had no effect on the naltrexone-insensitive (nonopioid) hypoalgesia, which occurred after 10 inescapable shocks, but completely blocked the naltrexone-sensitive (opioid) hypoalgesia, which followed 100 inescapable shocks. The stimulus prevented the development of the opioid hypoalgesia rather than merely masking its measurement. This effect did not depend on the use of lights-out as the stimulus but did depend on the temporal relation between the stimulus and shock. Stimuli immediately preceding or simultaneous with shock had no effect. Surprisingly, stimuli randomly related to shock also blocked the opioid hypoalgesia. Simultaneous measurement of both hypoalgesia and fear conditioned to contextual cues revealed that the level of fear did not predict the blockade of hypoalgesia. Different backward groups received different temporal gaps between shock termination and the signal. An interval between 2.5 s and 7.5 s eliminated the effect of the signal on fear, but 12.5-17.5 s were required to eliminate the effect of the signal on hypoalgesia. The opioid hypoalgesia blocking power of the random stimulus was entirely attributable to those stimuli occurring within 15 s of the termination of the preceding shock. The implications of these results for the explanation of stimulus feedback effects and for stress-induced analgesia are discussed.     

Predictability and controllability: Differential effects upon contextual fear

The independence of action of controllability and predictability has recently been questioned by research demonstrating that the effects of control over shock termination can be mimicked by feedback stimuli when a contextual fear measure is used. This suggests that the varied effects of controllability, particularly controllability of shock termination, may result not from controllability per se but from predictability of shock absence. The present experiments address this issue by examining whether controllability and predictability similarly affect contextual fear under several parametric conditions. In Experiment 1, control over shock termination was found to reduce contextual fear at an earlier point in training than prediction of shock absence. Experiment 2 demonstrated an effect of controllability under conditions in which the feedback effect is precluded. Experiment 3 examined the possibility that the group differences observed in the above experiments could be due to a potential difference in the conditionability of the response-produced stimulation and the external feedback stimulus. The outcome of this study makes it unlikely that this is the case, since no evidence of overshadowing of the feedback stimulus was observed on a test of its associative strength. These experiments suggest that the effects of controllability may not be reducible to those of predictability. Furthermore, they have important implications for theoretical proposals concerning the effect of feedback on contextual fear.     

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.     

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.     

Sign-tracking in aversive conditioning

Two experiments were conducted to determine if rats tend to avoid contact with a stimulus that signals the occurrence of shock and contact a stimulus that signals the nonoccurrence of shock. The conditioned stimulus was a 60-sec platform presentation, and the unconditioned stimulus was a 2-sec inescapable shock. In each experiment, the emphasis was on two types of Pavlovian pairings: forward pairing in which each platform presentation was followed by shock, and backward pairing in which each platform presentation was preceded by shock and followed by a lengthy shock-free interval. Experiment 1 showed that in comparison with Random and CS-only procedures, the backward procedure produced a significant increase in approach and contact with the platform, but the forward procedure failed to produce a significant decrease in contact with the platform. Experiment 2, in which all groups were roughly equated for baseline levels of platform preference, demonstrated strong effects of both forward and backward conditioning. The experiments provide evidence for an aversive sign-tracking system in which animals' tendencies to withdraw from or approach and contact a platform CS are determined by the Pavlovian contingencies which render it a reliable signal for the occurrence or nonoccurrence of shock.     

Factors affecting the measurement of classically conditioned fear in rats following exposure to escapable versus inescapable signaled shock.

Three experiments are reported in which rats first received 50 escapable or inescapable signaled-shock trials. Experiment 1 (n = 22) employed an acquired-drive paradigm and found inescapable shock subjects learned a hurdle-jump response to escape the signal less rapidly than did escapable-shock subjects. Experiment 2 (n = 24) employed a conditioned emotional response paradigm and found inescapable-shock subjects suppressed more when the signal was introduced in the appetitive bar-pressing task. Both experiments measured spontaneous activity immediately following conditioning and found no group differences. Experiment 3 (n = 39) employed the same activity task and found no difference between escapable- and inescapable-shock groups when the signal was introduced into the activity task. Both groups displayed less activity than a nonshock control group during the signal. The results suggest that lack of control over the shock in the conditioning phase did not result in an increase of conditioned fear. The results are discussed in terms of a learned active-inactive predisposition to respond.     

Reconsideration of the role of competing responses in demonstrations of the interference effect (learned helplessness)

In Experiment 1a, rats trained to escape shock by performing a 2-s inactive response were less impaired on a subsequent 2-way shuttle response than their yoked counterparts that received inescapable shock. In contrast, in Experiment 1b, rats trained to escape shock by performing a longer duration inactive response were more impaired on the subsequent escape task than their inescapably shocked counterparts. In Experiment 2, the results of Experiments 1a and 1b were replicated, and the inactive responses performed during pretreatment by both the escapable and inescapable shock groups were assessed and correlated with test stage 2-way shuttle escape performance. These activity data indicate that inactivity during pretreatment shock in both escapable and inescapable shock groups was a highly reliable predictor of subsequent 2-way shuttle performance, irrespective of the pretreatment shock contingency to which these Ss were exposed.     

Conditioned inhibition of fear: Evidence for a competing response mechanism

In two experiments, inhibitory conditioning was attempted by presenting a discrete CS in a neutral stimulus environment shortly following the termination of either shock (Experiment 1) or a second discrete CS which had been paired in a forward manner with shock (Experiment 2). Evidence of successful inhibitory conditioning was mixed in Experiment 1, where the properties of the CS were assessed within an escape-from-fear procedure. Postresponse presentations of the CS enhanced performance, whereas the presentation of the CS prior to responding did not have the expected degrading effect on performance. In Experiment 2, the inhibitory properties of the CS were assessed by combining this stimulus with an excitatory CS and presenting the compound to rats engaged in a water-reinforced licking response. Less response suppression was found in reaction to this compound relative to three separate comparison conditions, thus witnessing the success of the inhibitory-conditioning procedure used. The common assumption that inhibitory conditioning results from the nonreinforcement of a CS in a situation where reinforcement is expected, i.e., one which contains previously reinforced cues, is not supported by these data, for no previously reinforced cues were simultaneously presented with the CS during inhibitory training. The data are in agreement with a conditioned antagonistic-response interpretation of inhibitory conditioning.     

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.     

Transfer of conditioned appetitive stimuli to conditioned aversive excitatory and inhibitory stimuli

The transfer of Pavlovian appetitive stimuli to Pavlovian aversive stimuli was examined in three experiments. In Experiment 1, rats received appetitive (Ap) conditioning designed to establish a flashing-light stimulus as either a CS+, CSo, or CS? for food, or to maintain it as a novel stimulus for US-alone subjects. Then, the stimulus was employed as a signal for weak shock in conditioned-emotional-response (CER) training. Both acquisition and extinction results showed that the ApCS+ facilitated and the ApCS? retarded aversive excitatory conditioning relative to the ApCSo and US-alone controls. Experiment 2 replicated the findings of Experiment 1 with both a moderate and a severe shock in CER training. In Experiment 3, different groups received the same appetitive conditioning as before, but to a flashing-light stimulus which was then employed as a signal for no shock in CER training. The ApCS? facilitated and the ApCS+ retarded aversive inhibitory conditioning relative to ApCSo and US-alone controls. Collectively, these findings establish that, in Pavlovian conditioning, transfer of an appetitive CS to an aversive excitor or inhibitor is facilitated by maintaining the initial conditioning contingency.     

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.     

Warning signal termination and a feedback signal may not serve the same function

Three experiments were conducted to test the possibility that a feedback signal (FS) and warning signal termination (WST), while equally reinforcing in the avoidance learning situation, reinforce through different underlying mechanisms. The first experiment showed that the reinforcing properties of an FS are reduced more than those of WST when these stimulus changes are made unreliable by the presence of shock following a CR on specified trials throughout acquisition. Experiment 2 confirmed this effect on avoidance performance when only a few punishment trials were administered following asymptotic avoidance acquisition. Experiment 3 demonstrated this effect during avoidance extinction with and without the presentation of punishment trials between acquisition and extinction performance. The results provided no support for the expectancy explanation of avoidance learning and were interpreted as consistent with the assumption that WST reinforces by permitting fear to dissipate and that the FS reinforces through fear inhibition.     

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.     

Shock preexposure and the reduced effectiveness of shock

In three experiments experience with shock was shown to reduce the effectiveness of shock as a reinforcer or motivator. In Experiment 1 rats were given signaled shock in a box separate from the runway where they were subsequently punished. These rats were less suppressed by shock punishment than rats that had no previous shock experience. In Experiment 2 preshocked rats were less suppressed by punishment and were slower to learn an escape-avoidance response than nonpreshocked rats, whether the preshock was signaled or unsignaled. In Experiment 3 as number of CS-shock pairings increased, fear of the CS decreased as did fear of the context. These results suggest that some central adaptation process produced by experience with shock reduces the effectiveness of shock as a reinforcer whenever shock is used repeatedly. This is independent of other effects, such as context blocking, that can affect responding after shock preexposure.     

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.     

The costs and benefits of processing emotional stimuli during rapid serial visual presentation

Using a dual-target identification task during rapid serial visual presentation (RSVP), we examined facilitation and interference effects exerted by emotional stimuli. Emotionally arousing first targets (T1s) were encoded with higher accuracy than neutral T1s. At the same time, identification of a second neutral target (T2) was impaired reflecting a failure of disengaging attention from arousing T1s. Similar interference was triggered by arousing filler stimuli that were not voluntarily searched for in the RSVP stream (Experiment 2). In Experiment 3, we showed that interference is reduced (though facilitation for arousing T1s is maintained) when the second task itself involves variations in emotional arousal. Vice versa, when arousal associated with the T2 stimulus was predictable, interference recurred (Experiment 4). Our findings indicate that the perceived emotional intensity of a stimulus is a determinant of successful identification during RSVP: Encoding of arousing stimuli is reliably facilitated. Interference effects with subsequent processing arise independently and are strongly modulated by the overall task context and specific processing strategies.