effects of punishing the coping response (conflict) on stress pathology ...

Journal of Comparative and Physiological Psychology 1971, Vol. 77, No. 1, 14-21

EFFECTS OF PUNISHING THE COPING RESPONSE (CONFLICT) ON STRESS PATHOLOGY IN RATS1 JAY M. WEISS2 Rockefeller University When rats avoid and/or escape electric shock that is preceded by a warning signal, little gastric ulceration normally develops under conditions used previously in this laboratory. In the present experiment, severe gastric ulceration developed under these conditions when animals were given a brief punishment shock each time they performed the avoidance-escape response, and thus were exposed to a conflict situation. Yoked "helpless" animals did not develop as much ulceration as avoidance-escape animals, showing that coping behavior can, under certain circumstances, be more ulcerogenic than helplessness. These results were predicted by a proposed theory which relates ulceration to certain psychological (or behavioral) variables. It is concluded that this theory and the notion of conflict do not constitute independent explanation but that the theory subsumes conflict. An explanation is derived for why conflict situations are particularly pathogenic.

This experiment examined the effects of being able to perform a coping response in comparison to being helpless, but under conditions where performance of the coping response produced a brief punishment. The experiment was conducted as follows: Rats were allowed to avoid and escape signaled electric shocks by turning a wheel while yoked animals received exactly the same shocks but could make no response which affected shock. These conditions were maintained throughout a 48-hr, stress session. However, during the second half (last 24 hr.) of the stress session, a brief pulse of shock was delivered each time the avoidance-escape subject turned the wheel, thereby punishing the correct response. The foregoing situation, in which the avoidance-escape animal must respond in order to terminate (or avoid) a highly aversive shock but consequently receives a brief shock for doing so, represents a conflict situation. Several previous experiments have investigated the physiological effects of conflict (Sawrey, Conger, & Turrell, 1956; Sawrey & Weisz, 1956; Weisz, 1957). In these studies, the conflict was established by shocking a hungry and thirsty animal

whenever it attempted to obtain food and/ or water. The subjects exposed to this conflict condition developed more stomach lesions than did subjects which were also food-water deprived and shocked but with no contingency between food-water seeking and shock. Whether this difference is due to conflict, however, has been questioned by several investigators (Miller, 1963; Moot, Cebulla, & Crabtree, 1970). One issue raised soon after the initial demonstration of this effect (Weisz, 1957) was the equality of shock in different groups. Sawrey et al. (1956) recognized that to show an effect of conflict, it was necessary to administer the same shock to animals not in conflict as was received by those in conflict, which had not been done in the Weisz study. Sawrey et al. adopted the ingenious procedure of wiring the shock grid of each conflict subject in series with the grid of a nonconflict animal. However, Miller (1963) pointed out that the use of grids still left open the possibility that conflict and nonconflict animals received different amounts of shock; for example, to reach the food, conflict animals had to advance across an electrified grid and therefore may have received intense shock through their sensitive front feet while nonconflict animals could have learned to remain on their haunches and so received less pain through their tougher rear feet. Since the variability of shock on a grid floor is apparently suffi-

1

This study was supported by United States Public Health Service _Research Grant MH-13189 from the National Institute of Mental Health. 2 Requests for reprints should be sent to Jay M. Weiss, Rockefeller University, New York, New York 10021. 14

CONFLICT AND STEESS PATHOLOGY

cient to reverse the effects of various conditions (e.g., Weiss, 1970), the potential for such variability indeed raises an important question. In addition to the shock problem, the early conflict experiments are also complicated because the subjects exposed to conflict may well have consumed less food than did subjects not exposed to conflict (see weight loss reported in Sawrey et al., 1956). Since food intake reduces ulceration (Hanson, 1963) and apparently did so in one conflict experiment (Ader, Tatum, & Beels, 1960), the ulcer differences reported could simply reflect differences in amount and/or timing of food intake. Indeed, food-intake differences are likely to have been important in these studies since a large percentage of the lesions appeared in the rumen, or noninnervated upper portion of the stomach. Such lesions, which have not occurred in my stress studies, are thought to develop in normal rats as the result of severe food deprivation (Robert & Nezamis, 1958; Shay, Komorov, Fels, Moranze, Gruenstein, & Siplet, 1945). If earlier conflict effects have been based on differential food intake, this would explain why Pare failed to find the effect when animals were responding for water (Pare, 1962) but did obtain the effect (and also found rumenal lesions exclusively) when animals were responding for food (Pare & Livingston, 1970) ? In the present experiment, the problems discussed above are not encountered be-

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cause (a) shock is delivered through fixed tail electrodes wired in series so that, regardless of condition, animals necessarily receive the same shock, and (b) conflict is established without using an appetitively motivated approach response so that all subjects can then be completely deprived of food during the experiment to eliminate any opportunity for food intake to influence the results. Relation of This Experiment to a Proposed Theory of Ulceration

In addition to investigating effects of conflict, the present experiment was also undertaken to test a prediction derived from the theoretical framework presented in Weiss (1971). In that paper, a schema was suggested which relates various behavioral (or psychological) factors to the development of gastric lesions. Using this theory, I attempted to derive a condition which, like the executive monkey experiment, would result in more pathology among animals able to perform a coping response than among helpless subjects. In none of the various conditions I have previously studied has such a result been obtained. The theory states that ulceration increases as relevant feedback from coping attempts (responses) decreases, relevant feedback being defined as the occurrence of stimuli that are not associated with the stressor. This predicts that a condition which should be even more ulcerogenic than the yoked or "helpless" condition, where the 3 To complete the review of previous conflict amount of relevant feedback from respondexperiments, an interesting study recently carried out by Moot et al. (1970) should be mentioned. ing is zero, is a condition in which the releThis study found that rats which could terminate a vant feedback from responding is below shock received when they bar pressed for food zero, or negative, which would occur if redeveloped little ulceration while rats exposed to sponses produce stimuli associated with the the same conflict situation but which could not terminate the shock ulcerated considerably. How- stressor. This prediction generated the proever, the latter group showed no more ulceration cedure of the present experiment in which, than did animals which simply received inescapable during the second half of the experiment, shock with no conflict present (no bar pressing for conditions were established whereby refood). Thus, the inescapable shock was apparently responsible for all ulceration, with the conflict sponses of the avoidance-escape animal contingency having no demonstrable effect. For would produce a negative amount of relethis reason, the study is mentioned here rather vant feedback since their immediate effect than in the discussion of conflict effects. The au- would be to produce the stressor itself (a thors correctly point out that what this experiment pulse of shock). Although the avoidance-esdid show was that being able to terminate shock results in less ulceration than being unable to do cape animals would receive considerable positive amounts of relevant feedback for so.

JAY M. WEISS

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responding during the first 24 hr. of the stress session, and even receive some positive feedback during the last half of the session from the cessation of shock albeit delayed, given that the immediate feedback consequences of responding would be negative for 24 hr., this condition should be extremely ulcerogenic. It should be pointed out that although the foregoing analysis in terms of feedback has been presented separately from the discussion of conflict, the concepts are not at all exclusive. The term conflict is simply a general description of a situation in which the consequences of responding (feedback) are, as specified in the previous paragraph, a mixture of positive and negative. The precise meaning of the term conflict, in fact, depends on specifying feedback consequences; thus, the theoretical structure presented above embodies a concept such as conflict but presents it in a specific operational form. METHOD Subjects The subjects were 72 male albino rats obtained from Hormone Assay Laboratories (Chicago, Illinois) and weighing 180-250 gm. at the time of the experiment.

Apparatus The apparatus was the same as described in Weiss (1971); it basically consisted of several small chambers, each of which had a wheel mounted at the front which the animal in the chamber could rotate. Each chamber was housed in a separate soundproof compartment.

Procedure

^

Three animals comprising a triplet were treated simultaneously. The three animals in each triplet, matched for body weight, were drawn from the colony and housed together without food for 24 hr. Each animal was then placed into a chamber and shock electrodes were attached to its tail as described previously (Weiss, 1971). Just before the first trial of the stress session, one subject of the triplet was randomly designated as the avoidanceescape subject, which controlled the frequency and duration of the shock by its responses; another was designated as the yoked subject, which received exactly the same shock as the avoidanceescape subject but had no control over shocks; and the third was designated as a nonshock control. The tail-shock electrodes of the avoidance-

escape and yoked subjects were wired in series so that the shocks received by these two subjects were identical in number, dtiration, and current throughout the entire experiment. The nonshock subject was never shocked throughout the entire experiment. A total of 24 triplets was used. The stress session was conducted using the parameters and procedures (tone signals, shock level, initial training of avoidance-escape subject, etc.) of the signaled shock condition as in Weiss (1971). In this condition, a beeping tone was presented 20 sec. before the shock. (The shock was delivered in pulses .2 sec. in duration with .4 sec. between pulses.) The avoidance-escape animal had control over shock by turning the wheel at the front of its cage. This response terminated any stimulus that was present (beep or shock) and postponed the onset of the next shock by 200 sec. Thus, this response would terminate shock, if shock had begun, and also avoid (or postpone) shock if made before shock occurred. The yoked animal received exactly the same stimuli (beep and shocks) as the avoidance-escape animal, but the wheel-turning response by the yoked animal had no effect on either beep or shock. Nonshock animals received the beep signal but no shock. This condition remained in effect for the first 24 hr. During the second 24 hr. of the experiment, the punishment contingency was introduced. The conditions remained exactly as they had previously except that whenever the avoidance-escape animal made the avoidance-escape response by turning the wheel at the front of its apparatus, activation of the response relay produced a single pulse of shock (.2-sec. duration). Thus, the avoidanceescape animal was required to respond in order to terminate the train of shocks which would otherwise begin 200 sec. after the last response; however, when it performed this response, it received a pulse of shock contingent on responding. The avoidance-escape animal could still respond before the shock to postpone the onset of the shock train and also to terminate the beep if it were present, but all such responses now resulted in a shock pulse. Yoked animals continued to receive exactly the same shocks as avoidance-escape animals, since their tail electrodes were wired in series, including all shock pulses that the avoidance-escape animals produced by responding. Twenty-four hours after the punishment contingency had been introduced (48 hr. after the session had begun), the animals were removed from their cages, weighed, and immediately sacrificed by decapitation. Blood was collected for determination of plasma corticosterone levels, which was carried out by the method of Guillemin, Clayton, Smith, and Lipscomb (1958). Each animal's stomach was opened and inspected for ulceration, and the ulcers were counted. Lesions were also measured (to the nearest .25 mm.), so that the total amount (length) of ulceration could be ascertained ; this constituted the principal measure of ulceration. Statistical analysis for all measures was based on

CONFLICT AND STRESS PATHOLOGY TABLE 1 MEDIAN NUMBER OP WHEEL-TURN RESPONSES AND SHOCKS RECEIVED BY ALL GROUPS DURING THE FIRST AND SECOND 24-HR. PERIODS OF THE STRESS SESSION Group 24-hr, period of stress session

Avoidanceescape

Yoked

2,505 350

479 350

48

1,245

1,192

16

415

415

Non-

First

Responses Shocks0 Second (punishment) Responses Shocks" • b

8 Since avoidance-escape and yoked animals are wired in series, the number of shocks received is necessarily identical in these groups. b "Punishment" shock pulses are not included.

signed-ranks tests for matched subjects. For details of stomach preparation, ulcer identification, and statistical analysis, see earlier papers (Weiss, 1968, 1971).

RESULTS Wheel-Turning Behavior (AvoidanceEscape Responding) Table 1 shows the median number of responses made by all groups during the first and second 24-hr, periods, and also the median shocks received. As expected, during the first 24-hr, period, when standard signaled avoidance-escape conditions were in effect, avoidance-escape animals made significantly more responses (p < .001) than yoked animals. During the second 24-hr, period, when each avoidance-escape response resulted in a pulse of shock, the responding of avoidance-escape animals diminished so that during this period avoidance-escape animals did not respond significantly more than yoked animals (p > .30). The number of shocks also increased in the second 24 hr. in comparison with the first 24 hr. Stomach Ulceration Gastric lesions were found in the glandular (lower) portion of the stomach. Figure la shows the total length of stomach lesions for all groups and the significance of com-

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parisons between groups. Figure Ib shows the same for number of lesions. It can be seen that when avoidance-escape animals received a brief pulse of shock for avoidance-escape responses during the last 24 hr. of the experiment, they developed more extensive stomach ulceration than did matched yoked animals which received the same shocks but without any relationship between responding and shock. Nonshock animals, as expected, showed less ulceration than avoidance-escape and yoked animals. Body Weight Loss and Corticosterone Concentration Figure 2a shows the amount of body weight lost during the stress session. The only significant differences for this measure were between nonshock and the other groups. Corticosterone levels are shown in Figure 2b. Under these punishment conditions, the plasma steroid concentration of avoidanceescape animals was higher than that of yoked subjects. Both shocked groups showed higher levels than nonshock animals. Significant correlations between amount of stomach ulceration and plasma I

I Non-shock Avoidance-escape I Yoked

Fia. 1. The median total length of gastric lesions (a) and number of lesions (b) for the nonshock, avoidance-escape, and yoked groups. Also shown are the confidence levels for all comparisons between groups for which the chance probability was .10 or less. Twenty-four triplets were used.

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JAY M. WEISS

FIG. 2. The median amount of body weight which subjects lost during the stress session and concentration of corticosterone in the blood at the conclusion of the stress session for the nonshock, avoidance-escape, and yoked groups. Also shown are the confidence levels for all comparisons between groups for which the chance probability was .10 or less. See Figure 1 for key.

corticosterone levels, as were observed in other experiments (Weiss, 1971), were found in the avoidance-escape group (r = .64) and the yoked group (r — .45), again showing the relationship between ulceration and endogenous steroid level. The subjects which showed very high steroid levels without exception showed very severe ulceration —those subjects having a steroid level over 70 jug. per 100-ml. plasma averaged 40.5 mm. of lesions. Water intake, which was also recorded during the stress session, did not differ in avoidance-escape animals (Mdn = 34.5 ml.) and yoked animals (Mdn = 33.0 ml.). Both shocked groups did drink more than nonshock animals (p < .001 in each case), which is again consistent with findings that water intake (in the absence of food) is increased in stressful situations (e.g., Deaux & Kakolewski, 1970; Weiss, 1971). DISCUSSION In the present experiment, conditions were found which produced more pathology in animals able to perform a coping response than in helpless animals. As a result

of receiving a brief pulse of shock whenever they performed a well-learned avoidanceescape response, avoidance-escape animals developed more severe stomach ulceration and showed higher corticosterone levels than did helpless (yoked) animals which received exactly the same shocks but could not perform the avoidance-escape response. Figure 3 shows the remarkable effect on ulceration. To the left is shown the ulceration which resulted in a normal signaled-shock condition in an earlier experiment. To the right are shown the present results obtained using the same conditions but with the punishment (or negative relevant feedback) contingency added during the second half of the experiment. These results therefore show that conflict, which describes the present avoidance-escape situation, can be extremely ulcerogenic, as Sawrey et al. (1956) have sug6.0r

o.o Signal

Signal + punishment

FIG. 3. On the left is shown the amount of ulceration (median length of lesions) which developed in the nonshock, avoidance-escape, and yoked group that was exposed to a stress condition in which the avoidance-escape and yoked animals received shock preceded by a warning signal (data from Weiss, 1971). On the right is shown the ulceration which developed in the same groups exposed to the same conditions except that a brief punishment shock pulse (negative relevant feedback) was administered to avoidance-escape and yoked animals whenever an avoidance-escape response was made during the second half of the stress session. See Figure 1 for key.

CONFLICT AND STRESS PATHOLOGY

gested. The findings of the present experiment, in conjunction with a proposed theory (Weiss, 1971), may provide some insight into why conflict is so ulcerogenic. This theory states that ulceration is a function of two variables: number of coping attempts, or responses, and amount of relevant feedback. Let us first examine the role of feedback in producing the present results. If we analyze the results shown in Figure 3, we can see how important response feedback was in determining the ulceration which developed in the punishment (or conflict) condition. Consider why the ulceration of avoidance-escape animals increased so strikingly in the punishment condition. First, it is apparent that the additional shock pulses received in the punishment condition (because of the response-shock contingency) had little effect on the amount of ulceration. This can be seen by comparing the two yoked groups, for the yoked animals in the punishment condition received all the additional pulses and developed only slightly more ulceration than the yoked animals in the normal signal condition, which of course received no such additional shock pulses. Therefore, if the additional shocks themselves did not cause the increased ulceration, what was the critical factor? Consider how these shocks altered the feedback from responses. For yoked subjects, the additional shock pulses had no effect on the feedback consequences from responding; that is, responses by yoked animals continued to have no effect on the occurrence of stimuli having any consistent relationship to the stressor, so that relevant feedback from responses remained at zero for these animals. But for avoidance-escape animals, the additional shocks altered the response feedback relationship drastically; whereas in the normal signal condition responses produced stimuli that were not associated with shock (relevant feedback was greater than zero), when the punishment shocks were added responses now produced stimuli that were associated with the stressor—in fact, responses produced the shock stressor itself—so that the amount of relevant feedback was now negative. As we can see in Figure 3, when feedback did not

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change, as in the yoked group, ulceration was very little affected, but when feedback changed from positive to negative, as in the avoidance-escape group, ulceration increased by more than 500%. Thus, it is apparent that the pathological nature of the conflict condition was determined not by the extra punishment shocks per se but by the relationship between responding and these shocks, or, in other words, the negative relevant feedback resulting from coping responses. If we now examine individual differences within the avoidance-escape (conflict) group, we can see that ulceration was a function of how much the animals responded under the negative relevant feedback condition. The number of responses avoidance-escape animals emitted under the negative relevant feedback contingency correlated .66 with the amount of ulceration these subjects developed. Of course, one might suggest that this simply demonstrates that animals which receive more shock (since a shock pulse resulted from each response) will develop more ulcers. Again, we can examine the ulceration of yoked animals to see that this is not correct. If the shock pulses themselves had produced the correlation, then the individual differences among yoked animals, which received the identical shock pulses, should also show a similar correlation between number of punishment shocks and ulceration. However, this correlation was very close to zero (r = —.07) in the yoked group. Thus, it is apparent that the positive correlation between ulceration and punished responding was not produced by the shock pulses per se but that the correlation clearly depended on the response-shock contingency, or the number of punished responses, in other words. The correlation indicates, therefore, that ulceration increased as the number of responses producing negative relevant feedback increased. Figure 4 shows a case illustrating this principle. To summarize the foregoing discussion, the results show that ulceration in a conflict situation (a) derives from very low (negative) relevant feedback for responding, and (b) becomes more severe as such responding

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JAY M. WEISS

FIG. 4. The stomach of a very severely ulcerated avoidance-escape animal which illustrates the relationship between responding in the punishment condition and the development of ulceration. This animal was essentially moribund when sacrificed. Its response rate during the period when the punishment contingency was in effect was higher than that of any other avoidance-escape subject. The amount of ulceration found in this subject was also greater than that seen in any other subject in this study.

increases. Thus, we see that conflict-induced ulceration is a function of two factors: feedback and responding. These are the two variables which form the basis of the proposed general theovy (Weiss, 1971) which attempts to account for the development of ulceration in stressfrl situations. Since the present experiment was generated from this theory and the results are consistent with its predictions, I believe that this framework encompasses conflict as well. According to this view, there is nothing qualitatively different about why ulceration develops in conflict situations as compared with other stress situations—animals ulcerate in conflict conditions, as in other stress conditions, because they make coping attempts for which relevant feedback is low. The pathogenic nature of conflict is thus said to derive from responding which produces low relevant feedback. What makes conflict situations particularly ulcerogenic is that they promote a large amount of low-feedback coping behavior. This occurs in two ways. First, in situations such as that of the present experiment, the animal must continually perform responses in order to terminate a very aversive condition even though the response is then consistently punished. Second, animals in all conflict sit-

uations characteristically vacillate before executing the punished behavior; that is, they will repeatedly approach and then withdraw from the shock grid to be crossed, the bar to be pressed, etc. Whereas a withdrawal response produces some positive relevant feedback, the approach response produces a comparable amount of negative relevant feedback, so that overall the relevant feedback from such behavior is zero. Moreover, the behavior fails to eliminate the stressor or alter the physical stimuli in the situation, so that this type of responding tends to continue. Since the present theory states that ulceration will develop to the extent that low-feedback responding occurs, we can see here a basis for ulceration in any conflict condition, including conditions in which conflict is induced by punishing an appetitively motivated approach response.* 4 This formulation predicts that if an animal ceases to respond in a conflict situation, it will not ulcerate. Miller (1964) insightfully surmised that one might alleviate certain ill effects of conflict not only by removing the punishment (i.e., negative relevant feedback) from the approach response but also by increasing the punishment enough to stop the animal from responding; the present analysis suggests that this should be indeed correct.

CONFLICT AND STRESS PATHOLOGY REFERENCES ADEB, R., TATUM, R., & BEELS, C. Social factors affecting emotionality and resistance to disease in animals: I. Age of separation from the mother and susceptibility to gastric ulcers in the rat. Journal of Comparative and Physiological Psychology, 1960, 53, 446-454. DEAUX, E., & KAKOLEWSKI, J. W. Emotionally induced increases in effective osmotic pressure and subsequent thirst. Science, 1970, 169, 1226-1228. GTJILLEMIN, R., CLAYTON, G. W., SMITH, J. D., & LIPSCOMB, H. S. Measurement of free corticosteroid in rat plasma: Physiological validation of a method. Endocrinology, 1958, 63, 349-358. HANSON, H. M. Restraint and gastric ulcers. Journal of Neuropsychiatry, 1963, 4, 390-395. MILLER, N. E. Animal experiments on emotionally induced ulcers. Proceedings of the Third World Congress of Psychiatry, 1963, 3, 213-219. MILLEB, N. E. Some implications of modern behavior theory for personality change and psychotherapy. In D. Byrne & P. Worchel (Eds.), Personality change. New York: Wiley, 1964. MOOT, S. A., CEBULLA, R. P., & CBABTREE, J. M. Instrumental control and ulceration in rats. Journal of Comparative and Physiological Psychology, 1970, 71, 405-410. PARE, W. The effect of conflict and shock stress on stomach ulceration in the rat. Journal of Psychosomatic Research, 1962, 6, 223-225. PARE, W. P., & LIVINGSTON, A. Brain norepinephrine and stomach ulcers in rats exposed to chronic

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conflict. Physiology and Behavior, 1970, 5, 215-220. ROBEBT, A., & NEZAMIS, J. E. Ulcerogenic property of steroids. Proceedings of the Society for Experimental Biology and Medicine, 1958, 99, 443-447. SAWREY, W. L., CONGEE, J. J., & TTIBBELL, E. S. An experimental investigation of the role of psychological factors in the production of gastric ulcers in rats. Journal of Comparative and Physiological Psychology, 1956, 49, 457-464. SAWBEY, W. L., & WEISZ, J. D. An experimental method of producing gastric ulcers. Journal of Comparative and Physiological Psychology, 1956, 49, 269-275. SHAY, H., KOMOBOV, S. A., PELS, S. S., MORANZE, D., GRUENSTEIN, M., & SIPLET, H. A simple method for the uniform production of gastric ulceration in the rat. Gastroenterology, 1945, 5, 43-61. WEISS, J. M. Effects of coping responses on stress. Journal of Comparative and Physiological Psychology, 1968, 65, 251-260. WEISS, J. M. Somatic effects of predictable and unpredictable shock. Psychosomatic Medicine, 1970, 32, 397-408. WEISS, J. M. Effects of coping behavior in different warning signal conditions on stress pathology in rats. Journal of Comparative and Physiological Psychology, 1971, 77, 1-13. WEISZ, J. D. The etiology of experimental gastric ulceration. Psychosomatic Medicine, 1957, 19, 61-73. (Received January 18, 1971)