effects of coping behavior in different...

Journal of Comparative arid Physiological Psychology1971, Vol. 77, No.<l, 1-13

EFFECTS OF COPING BEHAVIOR IN DIFFERENT WARNINGSIGNAL CONDITIONS ON STRESS PATHOLOGY IN RATS1

JAY M. WEISS2

Rockefeller University

Rats received electric shock that was preceded by either a warning signal, aseries of signals forming an "external clock," or no signal at all. In all con-ditions, subjects which could avoid and/or escape shock developed less ul-ceration than, did yoked "helpless" animals which received exactly the sameshock (through fixed electrodes wired in series) but had no control overshock. Presence or absence of a warning signal did, however, have an effect:A discrete warning signal reduced the ulceration both of subjects havingcontrol over shock and of yoked helpless subjects. A theory is proposedto explain how psychological factors determine the development of gastriculceration in stress situations, and the present results are examined in rela-tion to it.

In 1968 I reported that rats which couldavoid or escape electric shocks lost lessbody weight, developed fewer stomach ul-cers, and showed less fear in a stressful sit-uation (as measured by a CER test) thandid rats which received exactly the sameelectric shocks but could not avoid or escapethem (Weiss, 1968a). A previous studywhich had also examined the effects of cop-ing behavior on the development of psycho-somatic pathology obtained results oppo-site to these. Brady, Porter, Conrad, andMason (1958), in a study which becameknown as the "executive" monkey experi-ment (Brady, 1958), found that in fourpairs of monkeys, animals which couldavoid electric shocks eventually developedsevere gastrointestinal pathology and died,while animals which received the same elec-tric shocks but could not perform the avoid-ance response developed no discernible dis-orders. In the 1968a paper, I discussed thepossible reasons why my results were op-posite to those of Brady et al. Although thestudies in question were carried out on dif-ferent species, and there was an unfortunateselection factor in the executive monkey ex-periment (i.e., the avoidance and yokedsubjects were not chosen at random but,rather, a 2-4 hr. avoidance pretest was

'This study was supported by United StatesPublic Health Service Research Grant MH-13189from the National Institute of Mental Health.

2 Requests for reprints should be sent to Jay M.Weiss, Rockefeller University, New York, NewYork 10021.

given to each pair and the monkey respond-ing at the higher rate was always made theavoidance animal), nevertheless it wasplausible that the opposite results were duelargely to different experimental conditionsused in the two studies. The present experi-ment investigated this possibility.

This experiment examined the impor-tance of warning signals in the coping situ-ation. In the original studies I carried out,where the animal able to perform the cop-ing response developed less severe symp-tomatology than its helpless partner, theshock was always preceded by a tone sig-nal, a standard avoidance procedure. Thus,the tone always predicted the occurrence ofshock and could serve as a signal for theanimal to respond at the appropriate time.In the executive monkey experiment, on theother hand, shock was not preceded by asignal, for a Sidman avoidance schedulewas used. In this avoidance situation, theanimal postponed (avoided) shock witheach response but it had no external signalto inform it that shock was imminent so ithad to make a temporal discrimination inorder to predict when shock would occurand respond appropriately. This Sidmanavoidance response may be considerablymore difficult to maintain than is a signaledavoidance response; therefore, having tomaintain a coping response in an unsignaledshock situation might be more stressfulthan being unable to perform any effectiveresponse, whereas the reverse is true whenthe impending shock is clearly signaled. If

1

Copyright © 197J1 by the American Psychological Association Inc.

JAY M. WEISS

this were correct, it would afford an expla-nation for why the effects of coping behav-ior were opposite in my studies and in theexecutive monkey experiments.

In the present experiment, the effects ofthree different warning signal conditionswere studied. In each of these conditions,matched triplets of animals underwent ex-perimental treatment simultaneously, eachtriplet consisting of an animal which couldavoid or escape shock, a yoked animalwhich received exactly the same shocks(and warning signals) as the avoidance-es-cape subject but which had no control overshock, and a nonshock control animal. Inthe first warning signal condition, a signal(beeping tone) preceded shock by severalseconds, which formed a signaled coping-response situation for those subjects able toavoid and escape shock. In the second con-dition, no signal preceded shock, whichformed an unsignaled, or Sidman-type, cop-ing-response situation for avoidance-escapesubjects. In the third condition, called theprogressive-signal condition, the beep signalpreceded shock as in the first condition but,in this case, a series of tones, each increas-ing in frequency and amplitude, led up to

FIG. 1. The Plexiglas chamber, in which ananimal is performing the wheel-turning response inthe experimental situation. The tubing leadingfrom the top of the chamber is the air exhaustoutlet. The graduated cylinder seen in the rearcontains water; the drinking spout protrudes intothe chamber through a small hole.

the beep. Thus, animals in this conditionwere provided with an "external clock" giv-ing them even more information to predictthe occurrence of shock than was present inthe signal condition. The effect of these con-ditions was examined primarily upon thedevelopment of gastric ulcers. Steroid con-centration in the blood was also measuredsince steroids may participate in the ulcero-genic process. The amount of body weightlost during the stress session was observedas well.

METHOD

SubjectsThe subjects were 180 male albino Sprague-

Dawley rats obtained from Hormone Assay Labo-ratories (Chicago, Illinois). The animals weighedapproximately 180-250 gm. at the time of the ex-periment.

ApparatusThe apparatus consisted of individual Plexiglas

avoidance-escape chambers housed in soundproofcompartments (Industrial Acoustics, Inc., NewYork; Model AC-1) as shown in Figure 1. Thewheel at the front of the avoidance-escape cham-ber, when rotated by the animal, tripped a switchthat could be activated to produce escape from, oravoidance of, electric shock delivered to the tail.The shock source was a high-voltage ac step-uptransformer (1,200-v. peak output) with a 300 Kexternal resistance in series with the subjects, andthe current was varied by regulating the primaryvoltage input to the transformer. Auditory signalsoriginated from Ameco Code practice oscillatorsand were delivered through 4-in. Lafayette 8-ohmspeakers (No. 99-0172) with three speakers (onein each of three compartments) wired in parallel.

ProcedureAll experimental procedures were carried out si-

multaneously on three animals (a triplet). Thethree animals of each triplet were matched forbody weight (within 15 gm. of one another) whendrawn from the colony and were then housed to-gether in one cage where they had access to waterbut no food. Twenty-four hours later, each animalwas weighed and placed into a chamber inside anindividual soundproof enclosure (described above).Prior to each subject's being placed into its cham-ber, a lightweight aluminum disk was slipped ontothe animal's tail and a piece of tubing was securedto the tail behind the disk (see Figure 1); this as-sembly prevented the animal from pulling its tailcompletely into the chamber while permitting theanimal to turn over, move backward, and alsomove forward up to the point where the tubingcame in contact with the disk. Behind the disk andtubing, shock electrodes, consisting of two 2-cm.lengths of 18-gauge stainless-steel tubing, were

COPING BEHAVIOR AND STRESS PATHOLOGY

placed onto the tail after electrode paste wasrubbed lightly onto the site of electrode contact.The three subjects were then randomly assignedto three different groups, one being designated asthe avoidance-escape subject, which controlled thefrequency and duration of shock by its responses,another as the yoked subject, which received ex-actly the same shocks as the avoidance-escape sub-ject but had no control over shocks, and a non-shock control subject.8 The tail electrodes of theavoidance-escape animal and its matched yokedanimal were wired in series, so that the shocks re-ceived by these two subjects were identical in num-ber, duration, and current intensity throughout theentire experiment. The electrodes of the nonshocksubject were bypassed in the circuit so that thissubject was never shocked.

Warning signal conditions. Each triplet was alsoassigned randomly to one of the three warning sig-nal conditions (signal, progressive signal, no signal)which are diagrammed in Figure 2a. In the signalcondition, a beeping tone preceded shock by 20sec. The beep was produced by .1-sec. pulses of a555-cps tone with .3 sec. between pulses. In theprogressive-signal condition, shock was also pre-ceded by the beep as in the signal condition. Inthis case, however, an ascending series of tones oc-curred in the 180-sec. period prior to the beep. This180-sec. period was divided into six 30-sec. periods.Following the first 30-sec. period, during which notone occurred, the tones commenced, each lasting30 sec. and each increasing in frequency and ampli-tude with respect to the previous one. The fre-quencies for the ascending tones in this series were250, 275, 333, 385, and 555 cps. In the no-signal con-dition, no signal of any kind preceded shock.

The effect of these different warning signal con-ditions on the avoidance-escape schedules was asfollows: The basic response-shock contingency wasthe same in all three warning signal conditions. Inall conditions, if the avoidance-escape animalturned the wheel at the front of its apparatus, thesignal-shock sequence was immediately terminatedand begun again; i.e., the signal-shock sequencewas reset to the time marked "0" in Figure 2a.Thus, if shock had begun, a response terminatedshock immediately and delayed the next shock for200 sec.; if shock had not yet begun, the response

8 It is necessary to point out that the present ex-periment does not utilize the yoked-control designwhich has been criticized by Church (1964). Theyoked groups in the present experiment are in noway a control condition. "Yoked" is a specific con-dition in which animals receive shocks but have nocontrol over them. This is, in fact, precisely thepoint Church made: He correctly pointed out thatyoked is a specific condition in which animals arehelpless so that stimuli (or reinforcements) are im-posed on such animals regardless of their physio-logical state, level of arousal, etc. This condition is,of course, specifically one that I wished to studyin the present experiment, which was designed tocompare the effects of having a coping responsewith the effects that occur when no such responseis available and stimuli therefore occur arbitrarily.

postponed shock for 200 sec. An avoidance-escaperesponse therefore had the same effect on shockfrequency regardless of the warning signal condi-tion—the response always delayed the next shockfor 200 sec. A response, in resetting the signal-shocksequence, also immediately terminated any warn-ing signal (or CS) that was present, as is standardprocedure in signaled avoidance-escape situations.Thus, if an animal in the signal condition re-sponded during the beep prior to shock, the beepimmediately terminated, and if an animal in theprogressive-signal condition responded during oneof the ascending tones or the beep preceding shock,the tone or the beep immediately terminated. Fig-ure 2b shows the effect of the same hypotheticalresponse pattern on stimuli (tones and shocks) inthe signal condition (upper section), progressive-signal condition (center), and no-signal condition(lower). A total of 60 triplets (20 in each condi-tion) were used.

Stress-session procedure. At the beginning of thesession, the avoidance-escape animal received abrief period of training (30 min.) in wheel turning.The shock, which was administered in pulses (pulseduration, .2 sec.; interpulse interval, .6 sec.), waskept at a low intensity during this phase {not ex-ceeding 1.0 ma.). On the initial trials, the shockwas reduced or terminated whenever the avoid-ance-escape animal moved toward the wheel andincreased slightly when the animal moved awayfrom the wheel. Once the animal had learned toturn the wheel, the shock was set at a low level(.5-.6 ma.) for the remainder of the training pe-riod. Trials were presented at the rate of 1/minduring this training phase. It should be noted thatyoked animals, being wired in series with avoid-ance-escape animals, received all shocks that werereceived by avoidance-escape animals during allphases of the experiment, including the trainingperiod.

At the conclusion of the initial training period,standard conditions (as described in the previoussection on warning signal conditions) were initi-ated. The shock, delivered in pulses as describedin the previous paragraph, was initially set at anintensity of 1.6 ma., and every 12 hr. the intensitywas increased by .6 ma. The stress session lastedfor 48 hr. Water was available ad lib throughoutthe session, and the amount consumed was re-corded.

At the end of the stress session, the animalswere quickly removed from the apparatus, weighed,and sacrificed by decapitation. Blood was collectedfor plasma corticosterone determination, (Thetime required to remove an animal from the ap-paratus—from the opening of the compartmentdoor to decapitation—did not exceed 1 min., sothat steroid levels were not affected by the re-moval procedures.) Stomachs were removed,opened, and mounted for inspection (see Weiss,1968a, for details of the procedure).

Measures and StatisticsStomach ulceration was the primary stress symp-

tom measured in this experiment. Stomachs were

JAY M. WEISS

"Beep"Shock

Signal

No signal

30 60 90 120

Time (sec)

150 180 200

Signal

Response

Progressive signal

No signal

FIG. 2. At top (a) is shown the basic arrangement of warning signals and shock in the signal, pro-gressive, and no-signal conditions. At bottom (b) is shown the effect of one hypothetical avoidance-escape response pattern on shock and warning signals in each of these conditions.

examined under a dissecting microscope and le-sions were counted. The criteria for identificationof lesions by gross inspection of tissue can be foundin an earlier paper (Weiss, 1968a). Recent experi-ments (Ganguly, 1969; Sethbhakdi, Pfeiffer, &Roth, 1970) have demonstrated the importance ofquantifying the amount of the gastric mucosawhich is ulcerated, having shown that measureswhich do not reflect this are insensitive to differ-

ences produced by known ulcerogenic conditions.Therefore, the length of each lesion was measured,a method used previously in this laboratory (Weiss,1968a, 1970); the total length of lesions found ineach subject constituted the principal measure ofamount of ulceration. In addition to gastric le-sions, body weight change during the session andplasma corticosterone concentration at the time ofsacrifice were measured. Plasma corticosterone was


determined by the method of Guillemin, Clayton,Smith, and Lipsoomb (1958).

Statistical analysis was carried out using non-parametric tests of significance, since the scores onmost measures were not normally distributed. Thefollowing statistical tests were used: For compari-sons between avoidance-escape, yoked, and non-shock subjects of the same warning signal condi-tion, Wilcoxon signed-ranks tests for matched sub-jects were used. (Since one subject from each ofthese groups was included in each triplet, thesegroups all contained matched subjects.) For com-parisons between groups that were not of the samesignal condition, Mann-Whitney U tests were used.

RESULTS

Wheel-Turning Behavior (Avoidance-Escape Responding)

Table 1 shows the median number ofwheel-turning responses for all groups andthe median number of shocks received byanimals in each condition. As expected,avoidance-escape animals made signifi-cantly (at least p < .05) more responsesthan yoked animals in each signal condi-tion.

Avoidance-escape subjects showed a widevariety of response patterns, particularly inconditions where a signal preceded shock(signal and progressive-signal conditions).The total number of responses made byavoidance-escape subjects in the signal con-dition ranged from slightly over 1,500 tomore than 20,000, and the range was similarfor subjects in the progressive-signal condi-tion. Approximately 70% of the avoidance-escape animals in these two signaled-shockconditions did not often respond during thebeep signal preceding shock but respondedquickly after the shock began, thus termi-nating it; i.e., they primarily escaped fromshock. This accounts for the high number ofshocks in these conditions. The remaining30% of the animals in each of these condi-tions, on the other hand, consistently re-sponded during the beep prior to the shock,terminating this signal and avoiding theimpending shock. In the no-signal condi-tion, avoidance-escape animals also showedconsiderable variation in responding(range: 3,200-31,000 responses) but themost striking feature of this group was itsgenerally high response rate. These avoid-ance-escape animals made more responsesthan avoidance-escape subjects in the signal

TABLE 1MEDIAN NUMBER OF WHEEL-TURN RESPONSES

AND SHOCKS RECEIVED BY ALL GROUPSDURING THE STRESS SESSION

Condition

SignalResponsesShocks"

Progressive signalResponsesShocks'*

No signalResponsesShocks8

Group

Avoidance-escape

3,717705

4,418702

13,992516

Yoked

1,404705

2,678702

4,357516

Non-shock

60

74

51

a Since avoidance-escape and yoked animalsare wired in series, the number of shocks receivedis necessarily identical in these groups.

condition (p < .001) and progressive-signalcondition (p < .005), which accounts forthe lower number of shocks received by ani-mals in the no-signal condition. Yoked ani-mals in the no-signal condition also showedmore wheel-turning behavior than yokedanimals in the signal condition (p < .001)but not significantly more than yoked sub-jects in the progressive-signal condition.

Stomach UlcerationGastric lesions, commonly called stress

ulcers, were found in the lower, glandulararea of the stomach. Figure 3 shows such alesion as it appeared in the stomach, andalso a histological section of this lesion. Nolesions were found in the upper, rumenalarea of the stomach.

Figure 4 shows the amount of lesionedgastric tissue (length of lesions) found ineach group, and the confidence levels for allsignificant comparisons. Figure 5 shows thesame for number of lesions.

Within all three signal conditions, avoid-ance-escape animals showed less extensivegastric ulceration than did yoked animals.The difference between the avoidance-es-cape and yoked groups was statistically sig-nificant in each condition on at least one ofthe two measures, with the largest differ-ence between these groups clearly occurringin the progressive-signal condition. Non-shock animals, which developed a small

JAY M. WEISS

. i •

•xar

FIG. 3. At top is shown a gastric lesion (indi-cated by arrow) as it appeared in a rat's stomach.The lesion lies in the lower, glandular part of thestomach. The upper, rumenal part of the stomach,which has not been removed in this case, shows nolesions, as usual. At bottom is shown a histologicalsection of the lesion seen above.

amount of ulceration as a result of the 48-hr, restraint in the apparatus, showed lessulceration than the animals which receivedshock (avoidance-escape and yokedgroups), as expected.

Examining differences between warningsignal conditions showed that avoidance-es-cape animals developed more ulceration inthe no-signal condition than they did in ei-ther the signal or progressive-signal condi-tion, in which avoidance-escape animals de-veloped similar amounts of ulceration.Thus, animals able to avoid and escapeshock developed more ulceration whenshock was not preceded by a signal thanthey did when shock was signaled, though,as stated in the previous paragraph, in nocase did avoidance-escape animals developmore ulceration than matched yoked sub-jects. Comparing yoked animals across con-ditions, ulceration was also more extensivein the no-signal condition than it was in thesignal condition. Ulceration of yoked ani-mals in the progressive-signal condition,

however, was almost as severe as thatwhich occurred in the no-signal condition.

It should be noted that the ulceration ofavoidance-escape animals which consist-ently terminated the beep signal beforeshock did not differ markedly from thoseavoidance-escape animals in the same sig-nal conditions which did not do so. In thesignal condition, for example, the medianamount of ulceration for the entire groupwas 1.12 mm.; for subjects with a largenumber of beep terminations (150 or more;n = 5), it was 1.25 mm.

Body Weight Loss

Figure 6 shows body weight loss duringthe stress procedure for all groups. Yokedanimals in the progressive-signal and no-signal conditions lost significantly moreweight than did avoidance-escape animals;the weight loss difference between thesegroups in the signal condition was quitesmall and did not approach significance.Nonshock animals lost less weight thanshocked groups (avoidance-escape andyoked subjects) in all conditions.

5.0

4.0

o'</> 3.0

o 2.0

en 1.0 -

,0 0.0

I I Non-shock

HHl Avoidance-escape

•I Yoked

Signal Progressive No signalsignal

L.05J l.OOIJ1—.01—' '—.001—' i—.001—'L.05J HO-1 l.OOH

' .05 '' .01 '

-.05-

FIG. 4. The median total length of gastric le-sions for the nonshock, avoidance-escape, andyoked groups in the signal, progressive-signal, andno-signal conditions. Also shown are the confi-dence levels of all comparisons between groupsfor which the chance probability was .10 or less.Twenty matched triplets were used in each signalcondition.


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.9 6If)

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.y£ 4

.o£


HIO-1 L.OOIJ L.05J

'-.005-' '—.001-' ^-.001 —'HOH U05J '-.OH

i 005 '>- • • .05 '

-.01-

Fia. 5. The median number of gastric lesionsfor the nonshook, avoidance-escape, and yokedgroups in the signal, progressive-signal, and no-signal conditions. Also shown are the confidencelevels for all comparisons between groups for whichthe chance probability was .10 or less. See Figure4 for key.

Significance of comparisons across condi-tions are shown, but because of the variationin weight loss observed across conditions(e.g., compare nonshock groups), careshould be taken in interpreting differenceson this measure which are not based oncomparison of groups of the same signalcondition which had matched subjects.

It should be noted that prestress weight,which was taken prior to the placement ofthe animals into the apparatus for thestress procedure, was highly similar for allgroups. The average weight across the ninegroups of the experiment showed a range ofonly 3 gm.; the average weight of the light-est group was 212.5 gm.4 compared with215.5 gm. for the heaviest group; no differ-ence approached significance.

Plasma Corticosterone

Levels of plasma corticosterone at thetermination of the stress session are shownfor all groups in Figure 7. Individual varia-tion was considerable, which is not surpris-

* Weight includes the tail-guard assembly, whichwas in position on the tail when this weight wastaken. The entire assembly contributed approxi-mately 21.0 gm. to this weight. The animal did not,however, support the weight of the assembly inthe apparatus, as can be seen in Figure 1.

ing for the level of steroid in the blood,particularly under stress conditions (e.g.,Friedman, Ader, Grota, & Larson, 1967);for example, within the yoked group of thesignal condition, values ranged 6.3-102.0 /*g.per 100-ml. plasma. The only statisticallysignificant difference between matched sub-jects was the difference between nonshockand yoked animals in the no-signal condi-tion.

Plasma steroid level did, however, corre-late with amount of ulceration. The averagecorrelation for all groups which receivedshock (avoidance-escape and yoked sub-jects in each of the three signal conditions)was r = .52. This correlation was mainlyattributable to subjects with very high ster-oid levels which invariably showed exten-sive ulceration—in those subjects where thesteroid level exceeded 70 /j.g. per 100-ml.plasma, the amount of ulceration averaged21.2 mm.

Water IntakeIn all signal conditions, avoidance-escape

and yoked animals drank significantly (atleast p < .01) more water than nonshock

26 -


HOO& L.05J

i— .05—' i—.001—' '-.001—'KOIJ L05J KOHi jo '

-.10--.05-

Fia. 6. The median amount of body weightlost during the stress session by the nonshock,avoidance-escape, and yoked groups in the signal,progressive-signal, and no-signal conditions. Alsoshown are the confidence levels for all comparisonsbetween groups for which the chance probabilitywas .10 or less. See Figure 4 for key.

JAY M. WEISS

32 r

Signal Progressivesignal

No signal

-.05--.01-

FIG. 7. The median concentration of corticoster-one in the blood at the conclusion of the stresssession for the nonshock, avoidance-escape, andyoked groups in the signal, progressive-signal, andno-signal conditions. Also shown are the con-fidence levels for all comparisons between groupsfor which the chance probability was .10 or less.See Figure 4 for key.

animals, which is consistent with findingsthat water intake (in the absence of food)is increased when animals are exposed tostressful conditions (e.g., Deaux & Kako-lewski, 1970). In the progressive-signal con-dition, yoked animals drank more water(Mdn = 40.0 ml.; p < .02) than did

matched avoidance-escape subjects (Mdn= 33.0 ml.); no other significant differencewas found between avoidance-escape andyoked groups.

DISCUSSION

The present experiment showed that re-gardless of whether electric shock waspreceded by a warning signal, by a series ofwarning signals forming, so to speak, an ex-ternal clock, or by no signal at all, rats thatcould perform coping responses to postpone,avoid, or escape shock developed less severegastric ulceration than matched subjectswhich received the same shocks but couldnot affect shock by their behavior. Thus,altering the predictability of shock bymeans of external signals did not changethe basic effect of being able to perform acoping response compared with not beingable to perform one—being able to perform

an effective coping response was less patho-genic under all conditions studied. Thus, thepossibility discussed in the introduction—namely, that the absence of a warning sig-nal before shock might result in more pa-thology in animals able to avoid or escapeshock than in helpless yoked animals—wasnot borne out. Since the executive monkeyphenomenon, i.e., the occurrence of morepathology in avoidance-escape subjectsthan in yoked animals, was not found inany condition, the present results offer norationale for reconciling my earlier resultswith those of the executive monkey experi-ment. Instead, the present results, in combi-nation with earlier experiments, serve to es-tablish that the beneficial effect of copingbehavior in stressful situations is of consid-erable generality.

The present results point out again theextraordinary significance of psychologicalfactors in the production of stomach ulcers.If, in Figure 4, we compare the gastric ul-ceration of any nonshock group with that ofthe avoidance-escape animals in the signaland progressive-signal conditions, we cansee that simply receiving shock was not nec-essarily very harmful in and of itself.These avoidance-escape animals clearly ul-cerated more than did nonshock controls;however, the amount of ulceration in theseavoidance-escape animals was not verylarge. Now let us compare either of theseavoidance-escape groups with the yokedanimals in the no-signal condition. The dif-ference here was produced by psychologicalvariables, by differences in warning signalsand the ability to control shock, and not bythe presence or absence of the shock stres-sor, since all subjects in this comparison re-ceived shock (in fact, the yoked animals inthis comparison received 25% fewer shocksthan either of the avoidance-escapegroups). The size of this difference (evenignoring the difference in shock frequency)tells us that the psychological characteris-tics of the stressful situation—the predicta-bility, avoidability, and escapability ofshock—primarily determined how patholog-ical the stress situation was, not whetherthe animal was exposed to the stressor. Ihave noted this observation before (Weiss,1968a, 1968b, 1970); initially, it was sur-

COPING BEHAVIOR AND STRESS PATHOLOGY 9

prising but it has proved to be a consistentfeature of the results.

In regard to the other measures, theamount of body weight lost during thestress session by the various groups showeda pattern roughly comparable to that seenfor stomach ulceration. Significant differ-ences between avoidance-escape and yokedanimals, with yoked animals losing moreweight than avoidance-escape animals, ap-peared in the progressive-signal and no-sig-nal conditions, although this difference didnot reach significance in the signal condi-tion.

For plasma corticosterone levels, the var-iation between individual rats was so largethat this measure did not differentiate thegroups. This variation, however, makes thesteroid measure a good one for correlationalanalysis, and a correlation between steroidlevel and ulceration was observed which isof particular interest. Administration of ex-ogenous steroids, both in humans and inrats, often leads to gastric ulceration, so thatsteroids are thought to be involved in thecausal sequence by which gastric ulcera-tions develops (Roberts & Nezamis, 1964;Spiro & Milles, 1960). However, when exog-enous steroid is given, the quantity is oftenso large, the introduction of steroid into cir-culation is so abrupt, etc., that we wish toknow whether steroids secreted normally bythe adrenal cortex play a role in the ulcero-genic process. Results in the present experi-ment showed that very high endogenouslyproduced steroid levels were accompaniedby severe gastric ulceration; this lends sup-port to the possibility that steroids, inquantities that the animal is capable of se-creting, may contribute to the production ofulcers.

A THEORY TO EXPLAIN How COPINGBEHAVIOR AFFECTS ULCER

DEVELOPMENTWhile a number of significant conclusions

are clearly evident from the present results,puzzling aspects also remain. For example,why was the difference between avoidance-escape and yoked subjects consistentlylarger in the progressive-signal conditionthan it was in either of the other signalconditions? Based on data from the present

experiment, I have been able to generate atheory which attempts to answer this andother questions relating to how coping be-havior regulates the development of gastriculceration in stressful situations. The deri-vation of the hypotheses will not be pre-sented here; I shall simply state the theoryand show how it conforms to the presentresults.

Stress ulceration is said to be a functionof two variables: the number of coping at-tempts an animal makes, and the amount ofappropriate feedback which these copingattempts produce. Figure 8 shows how thesevariables interact. On the left side of thesolid line is represented the relationship be-tween the first variable, number of copingattempts, and ulcerogenic (ulcer-producing)stress. When an animal is presented with astressor, or stimuli associated (by contigu-ity) with the stressor, the animal will emitcoping attempts which we measure as re-sponses. The number of responses emittedand the amount of ulcerogenic stress di-rectly covary; that is, the more responseswe observe, the more likely the animal is todevelop ulcers. Hence, the first propositionis that ulceration tends to increase mono-tonically as the number of responses, orcoping attempts, increases.

The theory states, however, that expres-sion of the foregoing relationship is com-pletely dependent on a second variable—theconsequences of coping attempts, or, in op-

STRESSOR,

or stimuliassociated with

stressor

RESPONSES

ULCEROGENIC

STRESS

STRESSOR,


stressor

STRESSOR,


stressor

RESPONSE (S) RESPONSE(S)

Stimuli notassociated with

stressor

Stimuliassociated with

stressor

ULCEROGENIC

STRESS

FIG. 8. Factors which determine the presenceor absence of an ulcerogenic condition.

10 JAY M. WEISS

FIG. 9. At top (a) is shown the three-dimen-sional figure which describes the proposed rela-tionship between responses, feedback, and ulcera-tion. This relationship is a plane which shows howthe two independent variables, responses and feed-back, are related to the dependent variable, ul-ceration. At bottom (b) is shown how this planeis used. Where a hypothetical number of responses

erational terms, the stimulus feedback fromresponses. The effect of this variable isshown on the right side of the solid line inFigure 8. If responses immediately producestimuli that are not associated with thestressor, ulcerogenic stress will not occur. If,on the other hand, responses fail to producesuch stimuli, then ulcerogenic stress willoccur. Stimuli that are not associated withthe stressor and that follow a response arecalled relevant feedback, since their occur-rence is said to negate ulcerogenic stress.Thus, the more the relevant feedback, i.e.,the more responses produce stimuli that arenot associated with the stressor, the less theulceration. The second proposition is,therefore, that ulceration tends to decreasemonotonically as the amount of relevantfeedback from coping attempts increases.

Combining these two propositions gener-ates a function (a plane) such as is shownin Figure 9a. Figure 9b shows how, giventhe number of responses which an animalmakes and the amount of relevant feedbackit experiences from these responses, we canpredict the amount of ulceration which willdevelop. Where number of responses andamount of feedback intersect, we simplyproject upward until we reach the plane;the height of this point represents theamount of ulceration which occurs.

This theory generates some interestingpredictions. First, if an animal does notmake coping attempts, it will not ulcerateregardless of what the feedback circum-stances are. (See in Figure 9 that at allfeedback values intersecting with "zero"responses, the plane shows no elevation.)Also, if relevant feedback is maximallyhigh, an animal will not ulcerate regardlessof how many responses it makes. (See inFigure 9 that at all response values inter-secting with maximally high feedback, the

and amount of feedback intersect, the amount ofulceration is determined by the height of the planeabove this point. (For ease of reading this figure,responses and feedback are labeled across the axesin the foreground. These labels are customarilyplaced along the axes in the background which areparallel to the ones bearing the labels. It thereforeshould be noted that feedback designations applyto the axis from Point A to the intersection of thethree axes, and response designations apply to theaxis from Point B to the intersection.)


plane also shows no elevation.) As numberof responses increases and amount of feed-back decreases, the point where these quan-tities intersect moves closer and closer tothe intersection of the three axes, abovewhich the plane progressively rises higher,denoting that ulceration is expected to be-come progressively more severe.

To apply this framework, it is necessaryto keep clearly in mind what is meant byrelevant feedback. The principle to be re-membered is that relevant feedback consistsof stimuli which immediately follow a re-sponse. The amount of relevant feedback isthe extent to which a response producesstimuli that are not associated with thestressor. To avoid the stressor is not rele-vant feedback; in fact, more relevant feed-back will occur from escape responses thanfrom many types of avoidance responses.For example, in the present experiment thestimulus event of shock termination is fur-ther removed in time from the onset of theshock (i.e., less associated with the stressor)than is any other external stimulus in theenvironment (see Figure 2b). Moreover,shock termination is a very large change inthe external stimulus situation and is,therefore, an extremely conspicuous event.These factors make shock termination ex-cellent feedback, and this results fromevery escape response. In contrast, considerthe feedback from avoidance responses inthe no-signal condition. These responsespostpone shock, thus producing kinestheticand proprioceptive stimuli from respondingwhich are always at least 200 sec. removedfrom the onset of shock (good feedback),but such responses produce no change at allin the external stimulus situation; hence,the amount of feedback from this type ofavoidance response is considerably less thanthat of an escape response even though itavoids the stressor.

Figure 10 shows the present results in re-lation to the framework I have suggested.One can fix the position of any group withregard to the two important variables (re-sponses and feedback) since the respondingof each group was directly measured andthe amount of feedback in each conditioncan be ascertained, which is done as fol-

lows: The best response feedback occurredfor avoidance-escape animals in the pro-gressive-signal condition. In this case, anyresponse made more than 30 sec. after shockterminated a tone of some sort and immedi-ately produced a stimulus condition (si-lence) which was not closely associatedwith the onset of shock. The only responsesin this condition that failed to produce rele-vant feedback via external stimulus changewere those that occurred within the first 30sec. after shock. Avoidance-escape animalsin the signal condition experienced lessfeedback than this since responses made be-fore the beep produced no external feedbackevent in this condition. Nevertheless, feed-back in the signal condition was quite good;relevant feedback from external stimuli didarise from responses which terminated thebeep signal and, moreover, most animals inthis condition responded to terminate shock,which provided excellent feedback as ex-plained in the previous paragraph. The poor-est feedback for avoidance-escape animalsoccurred in the no-signal condition. In thiscase, only escape responses provided sub-stantial relevant feedback since responsesprior to shock produced no external feed-back, as explained in the previous para-graph. As a result, most of the responsesmade in the no-signal condition producedrather low feedback. Turning to the yokedanimals, their responses, by definition, hadno effect on external stimuli and so couldnot produce any stimuli consistently unre-lated to the stressor; relevant responsefeedback for all such groups is zero. In Fig-ure 10, all groups lie along the appropriatefeedback coordinate at points correspondingto the amount of responding which theyshowed. At these points, the amount of ob-served ulceration is indicated by the heightof each bar. The correspondence of thesevalues with the theoretical function can beassessed by comparing their fit with thefunction in Figure 9. We can now see why,for example, the difference between avoid-ance-escape and yoked animals was so largein the progressive-signal condition, for ani-mals in this condition made a substantialnumber of responses, with very good feed-back occurring for avoidance-escape sub-

12 JAY M. WEISS

AvoidanceNo signalProgressive signalSignal

FIG. 10. The figure shows the results obtained in the present experiment in relation to the proposedtheory. For each group which received shock, the amount of ulceration (height of bar) is shown at thepoint where responding and feedback for that group intersect.

jects in contrast to the zero feedback foryoked subjects.5

5 It is important to note that the small amountof ulceration which developed in nonshock controlanimals is not an exception to the theory set forthabove but is also explained by using the same prin-ciples. A minimum stress condition was imposedon all subjects, including nonshock controls, sinceall subjects were restrained in the apparatus for 48hr. without food. Any attempt that a subject madeto get out of this stressful situation necessarilyproduced zero relevant feedback because no re-sponse ever produced escape from the chamber(i.e., no response produced any stimuli that werenot associated with the chamber). Since attemptsto escape from the apparatus produce zero feed-back, simply being in the experimental situation is,according to the proposed theory, potentially ul-cerogenic, and subjects will ulcerate in accordance

One of the most significant aspects of thetheory proposed is that it does away withany qualitative distinction between animalswhich can avoid and escape shock and ani-

with the number of escape attempts emitted. Itwas found, in fact, that the wheel-turning behaviorof nonshock control subjects, which would reflectescape attempts, correlated with the amount of ul-ceration these subjects developed (r — .66). Thus,the ulceration of nonshock animals can be seen todevelop as a function of coping attempts for whichfeedback is low, and consequently fits into theframework presented above. If we examine Figure9, it is equally evident why the ulceration of non-shock groups was quite mild since, in the absenceof the major stressor of electric shock, the numberof responses emitted by these subjects was verylow.


mals which are helpless; the difference be-tween such conditions is expressed quanti-tatively. If we consider the two dimensionswhich are functionally related to ulceration(responding and feedback), we see thatavoidance-escape and yoked groups differquantitatively with respect to both—thesegroups differ in the amount of responsesthey emit and in the amount of relevantfeedback these responses produce. Thus, wecan incorporate both avoidance-escape andyoked (helpless) conditions into a commonschema, which we see done in Figure 10.The primary distinction between an avoid-ance-escape condition and a yoked condi-tion lies along the feedback continuum; foryoked, or helpless, animals, relevant feed-back for responding is zero, while for avoid-ance-escape animals, feedback occurs insome amount greater than zero dependingupon the stimulus characteristics of the sit-uation. This difference explains why ani-mals which have control over a stressorgenerally ulcerate less than do helpless ani-mals: Animals which have control generallyreceive a considerably greater amount ofrelevant feedback for their coping attemptsthan do helpless animals. Thus, the value ofcontrol for ameliorating ulcerogenic stress issaid to lie essentially in the ability to pro-duce relevant feedback from responses. Us-ing this approach, we can analyze a widevariety of circumstances and predict theireffects, which has been done in generatingfurther experiments (Weiss, 1971a, 1971b).

REFERENCES

BRADY, J. V. Ulcers in "executive" monkeys. Scien-tific American, 1958,199, 95-100.

BRADY, J. V., PORTER, R. W., CONRAD, D. G., &MASON, J. W. Avoidance behavior and the de-velopment of gastroduodenal ulcers. Journalof the Experimental Analysis of Behavior,1958, 1, 69-72.

CHURCH, R. M. Systematic effect of random errorin the yoked control design. PsychologicalBulletin, 1964,62, 122-131.

DEAUX, E., & KAKOLEWSKI, J. W. Emotionally in-duced increases in effective osmotic pressureand subsequent thirst. Science, 1970,169, 1226-1228.

FRIEDMAN, S. B., ADER, R., GROTA, L. J., & LARSON,T. Plasma corticosterone response to parame-ters of electric shock stimulation in the rat.Psychosomatic Medicine, 1967, 29, 323-328.

GANGULY, A. K. A method for quantitative assess-ment of experimentally produced ulcers in thestomach of albino rats. Experientia, 1969, 25,1224.

GUILLEMIN, R., CLAYTON, G. W., SMITH, J. D., &LIPSCOMB, H. S. Measurement of free corti-costeroid in rat plasma: Physiological valida-tion of a method. Endocrinology, 1958, 63,349-358.

ROBERT, A., & NEZAMIS, J. Histopathology of ste-roid-induced ulcers. Archives of Pathology,1964, 77, 407-423.

SETHBHAKDI, S., PFEIFFER, C. J., & ROTH, J. L. A.Gastric mucosal ulceration following vasoac-tive agents: A new experimental approach.American Journal of Digestive Diseases, 1970,15, 261-270.

SPIRO, H. M., & MILLES, S. S. Clinical and phys-iologic implications of the steroid-induced pep-tic ulcer. New England Journal of Medicine,1960, 26, 286-294.

WEISS, J. M. Effects of coping responses on stress.Journal of Comparative and PhysiologicalPsychology, 1968, 65, 251-260. (a)

WEISS, J. M. Effects of predictable and unpredic-table shock on development of gastrointestinallesions in rats. Proceedings of the 76th AnnualConvention of the American Psychological As-sociation, 1968, 3, 281-282. (b)

WEISS, J. M. Somatic effects of predictable andunpredictable shock. Psychosomatic Medicine,1970, 32, 397-408.

WEISS, J. M. Effects of punishing the coping re-sponse (conflict) on stress pathology in rats.Journal of Comparative and Physiological Psy-chology, 1971, 77, 14-21. (a)

WEISS. J. M. Effects of coping behavior with andwithout a feedback signal on stress pathologyin rats. Journal of Comparative and Physio-logical Psychology, 1971, 77, 22-30. (b)

(Received January 18, 1971)

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