The Psychlgical Recrd, 1999, 49, 211-220 DIRECTED FORGETIING: SHORT-TERM MEMORY OR CONDITIONED RESPONSE? WENDY S. MILLER and HARVARD L. ARMUS The University f Tled Previus researchers have interpreted the phenmenn f directed frgetting in terms f animal shrt-term memry and rehearsal. An alternative explanatin-that directed frgetting is attributable t the respnse r nnrespnse t a sequence f stimuli-is prpsed and tested with rats. Rats were tested fr directed frgetting using a variatin f the standard directed frgetting task, in which the sample was fllwed by either a remember cue r a frget cue, and in which there was a secnd cue immediately befre the presentatin f the cmparisn stimuli. Results appear t supprt the memry and rehearsal explanatin f directed frgetting. Delayed matching t sample (DMTS) is a cmmnly used prcedure fr studying animal shrt-term memry. The basic prcedure f a DMTS task is that ne f tw stimuli ccurs at the beginning f a trial, and then after a delay, the animal must chse between tw different stimuli. The first stimulus is referred t as the sample stimulus, and the secnd tw stimuli are referred t as the cmparisn stimuli. Reinfrcement is cntingent upn the animal chsing the crrect cmparisn stimulus, that is, the ne that matches the sample stimulus it saw befre the delay. Many researchers have used the DMTS task t study animal shrtterm memry (Grant, 1981 ; Leith & Maki, Jr., 1975; Maki, 1979; Maki & Hegvik, 1980; Maki, Olsn, & Reg, 1981; Santi & Savich, 1986; Stnebraker, Rilling, & Kendrick, 1981). Typically, animal shrt-term memry has been studied by adding "remember" and ''frget'' cues (Rcues and F-cues, respectively) t the task immediately fllwing the presentatin f the sample stimulus. After the delay, the cmparisn stimuli are presented n trials in which the R-cue had been presented, but they are nt presented n trials in which the F-cue had been presented. Frgetting is assessed by presenting ccasinal prbe trials, Crrespndence cncerning this article shuld be addressed t Wendy S. Miller, Department f Infrmatin Technlgy, The University f Tled, Tled, OH 43606. E-mail may be sent via Internet t wmiller@utnet.utled.edu.
212 MILLER AND ARMUS in which the cmparisn stimuli are presented n trials in which the F cue fllwed the sample stimulus. Accrding t the rehearsal hypthesis, the R-cue initiates rehearsal f the sample stimulus during the delay perid, and the F-cue serves as a signal t the animal that it is nt necessary t rehearse the sample stimulus during the delay perid. Thus, directed frgetting is generally defined as a perfrmance decrement n prbe trials (in which the cmparisn stimuli fllw the F cue) as cmpared t perfrmance n R-cue trials (in which the cmparisn stimuli fllw the R-cue). Maki and Hegvik (1980) supprted the rehearsal hypthesis f directed frgetting; their pigens shwed prer perfrmance n F-cue prbe trials than n R-cue trials. Santi and Savich (1986), als studying pigens, manipulated the placement f the R- and F-cues within the delay perid. They fund that when the R-cue was placed further int the delay perid, matching accuracy decreased. Timing f the F-cue, hwever, did nt affect matching accuracy. Santi and Savich cncluded that "pigens actively maintain r rehearse infrmatin derived frm the sample stimulus during the retentin interval," (p. 368), and that "R cues can initiate and maintain rehearsal." (p. 369). Grant (1981) studied the effect f tw-cue prbe trials n directed frgetting. He fund that n prbe trials in which the R-cue immediately fllwed the F-cue, accuracy went up, relative t prbe trials where nly the F-cue was presented. On prbe trials in which the F-cue immediately fllwed the R-cue, the F-cue reduced the effectiveness f the R-cue. Grant cncluded that the animals actively rehearse after the presentatin f the R-cue and that they learn t frget (r t nt rehearse) after the presentatin f the F-cue. Stnebraker, Rilling, and Kendrick (1981) manipulated the timing f the R- and F-cues within the delay perid. They fund that if the R-cue immediately fllwed the F-cue after the presentatin f the sample stimulus, the R-cue effectively "canceled ut" the F-cue. That is, matching accuracy increased relative t trials in which the R-cue did nt fllw the F-cue. Hwever, when the F-cue was presented at the beginning f the delay and the R-cue was nt presented until the end f the delay, matching accuracy went dwn relative t trials in which the R cue was presented alne. The R-cue in this situatin did nt cancel ut the effects f the F-cue. Stnebraker et al. als nted that in prbe trials in which the R-cue fllwed the F-cue, matching accuracy never reached the level that it did n regular R-cue trials, meaning that this cancellatin was incmplete. There seems t be a prblem with the cnclusins drawn by these investigatrs (Grant, 1981; Maki & Hegvik, 1980; Maki et ai., 1981; Stnebraker et ai., 1981); namely, that this may nt be directed frgetting at all, but may simply be the learning t respnd r nt t respnd t a cmplex sequence r chain f stimuli. In ther wrds, perhaps the "remember" and "frget" cues are instead learned as the "respnd" and "dn't respnd" cues. If the animal has learned t respnd
SHORT-TERM MEMORY OR CONDITIONED RESPONSE 213 nly t the R-cue, then, during prbe trials, in which the animal is presented with the cmparisn stimuli after the F-cue, it des nt knw hw t respnd; hence, the prer perfrmance n prbe trials. If "directed frgetting" is indeed simply a learned respnse t a sequence f stimuli, then the animals will respnd (r respnd apprpriately) nly after the presentatin f the R-cue. Fr this reasn, ne type f prbe trial in the present experiment cntained the presentatin f the F-cue, fllwed by a delay, fllwed by the presentatin f the R-cue, fllwed by the presentatin f the cmparisn stimuli. Prbe trials were als intrduced which cntained the presentatin f the R-cue, fllwed by a delay, fllwed by the presentatin f the F-cue, fllwed by the presentatin f the cmparisn stimuli. Fr cmparisn, a third type f prbe trial mirrred the prbe trials in the Maki and Hegvik (1980) experiment, in which the F-cue was simply fllwed by a delay, which was then fllwed by the cmparisn stimuli. The scres n these three types f prbe trials were cmpared t the scres n the tw types f R-trials in the final analysis. If, as suggested by the rehearsal explanatin, presentatin f the F cue after the sample stimulus inhibits rehearsal f the sample, then the additin f an R-cue n the prbe trials after an F-cue and a delay shuld have n effect. The animals shuld still perfrm mre prly n these prbe trials than n the regular trials, in which the cmparisn stimuli are presented after the presentatin f an R-cue. In the prbe trials in which an R-cue precedes the delay and an F-cue, the animals shuld perfrm just as well as they did n the regular trials, because the rehearsal has already taken place, and the additin f an F-cue immediately befre the presentatin f the cmparisn stimuli shuld nt affect this rehearsal. If, hwever, the pr perfrmance n prbe trials in the riginal experiment was caused, nt by the absence f rehearsal, but by the learning t respnd r nt respnd t a sequence f stimuli, animals shuld d just as well n prbe trials in which an R-cue is presented after an F-cue as n regular trials, because the stimulus t respnd (the R-cue) is presented t them immediately befre the presentatin f the cmparisn stimuli. On prbe trials in which an R-cue precedes an F cue, hwever, perfrmance shuld decrease relative t the perfrmance n R-cue trials, because the last cue presented t the animals was the cue t nt respnd. In ther wrds, the predictins frm the hypthesis that directed frgetting is because f a learned respnse t a chain f stimuli and the hypthesis that directed frgetting is attributable t directed rehearsal r nnrehearsal are ppsite fr bth the prbe trials in which the R-cue fllwed the F-cue and prbe trials in which the F-cue fllwed the R-cue. Methd Subject Twenty experimentally naive, male, Lng-Evans strain rats,
214 MILLER AND ARMUS apprximately 120 days ld, were used as subjects. During training, 4 f the animals died frm illness unrelated t the experiment, and 7 did nt learn the task, leaving 9 testable subjects. Apparatus The apparatus was an perant chamber apprximately 30 cm n a side, with tw 4-cm-wide levers munted parallel t the frnt wall f the chamber, 8 cm abve the flr, and 5 cm frm the left and right sides f the chamber. The levers extended apprximately 1.5 cm int the bx. A 2.8-W signal light was munted abve each lever. There were fur huse lights, which culd be illuminated in cmbinatin t prduce a lw level (apprximately 1.5 ft-candles), a medium level (apprximately 17.5 ft-candles), and a high level (apprximately 41 ft-candles) f illuminatin. The stimuli and levers were cntrlled by Apple lie cmputers, which were als used t recrd respnses. Frty-five-mg Nyes pellets were used as reinfrcement. Prcedure Nine days prir t pretraining, animals were placed n a deprivatin diet f 1.5 hr f access t fd per day, with ad lib access t water. On the last day prir t pretraining, the animals were fed five 45-mg Nyes pellets 5 min befre their regular feeding time. Pretraining. Animals were first trained t press the levers, either lever delivering ne 45-mg Nyes pellet t the fd cup. The lights ver the levers were illuminated during the entire daily sessin. During the next phase f pretraining, bth levers were retracted fr 2 s immediately after each respnse. Frm this pint n, thrughut the entire experiment, if bth levers were in the bx, bth levers retracted after either lever was pressed, and if nly ne lever was in the bx, it retracted after it was pressed. The rats were next trained t press nly the lever that had the light n ver it by presenting nly the crrect lever (the ne with the illuminated signal light ver it) fr 27 days. During the next phase, ne f the signal lights came n fr 5 s, and then bth levers were presented at the ffset f the signal light. The animals were rewarded nly if they pressed the lever which had had the light n ver it. When the animals had reached a criterin f 80% crrect fr 4 ut f 5 cnsecutive days,1 the next phase was begun. This invlved intrducing a delay between the ffset f the light (the sample stimulus) and the presentatin f the levers (the cmparisn stimuli). The delay was.5 s the first day, and it was gradually increased t 5 s. When the animals reached a criterin f at least 80% crrect fr 4 ut f 5 cnsecutive days, regular trial training, with the R- and F-cues (huse light dimmed and huse light brightened fr 1. 5 s, cunterbalanced), was begun. Training trials. There were fur types f regular trials, which were presented in a randm rder t each f the animals fr 200 trials per day fr 27 days: 1 Except fr Rat #41, wh had at least 65% crrect fr 3 ut f 5 cnsecutive days.
SHORT-TERM MEMORY OR CONDITIONED RESPONSE 215 1. Type R: sample stimulus (ne f the lights ver ne f the levers), R-cue (brightening f the huse light fr 5 animals, and dimming f the huse light fr 4 animals), 5 s delay, cmparisn stimuli. 2. Type F: sample stimulus, F-cue. At this pint, the F trials ended. 3. Type RR: sample stimulus, R-cue, delay, a secnd R-cue, cmparisn stimuli. 4. Type FF: sample stimulus, F-cue, delay, a secnd F-cue. At this pint, the FF trials ended. (See Figure 1 fr a schematic representatin f the fur types f regular trials.) Typ. R Trials Sample stimulus --------. R.cue 1 5-s.. d.l.y '---_---'I I <- -,I ::IOD.Ii Typ. lit TrWs S.",p1e IIlmulu. 1 5... d.l.y.. R. cae r-------- R cue '---_--'I <-I -,I ::SOD Reinfrcement N n:jdfrccmcdt Reinfrcement N reinfrcemcnt.ii Type FTrials Sample stimulus. F CDC 1 5-... d.l.y.ii. Type FF TrI.l. S.",pl. stimulus F cuc 1 5-10. d.l.y F... Trial.udl. Trial.uds. Figure 1. Schematic representatin f the fur types f training trials. R = Remember training trials, RR = Remember-Remember training trial, F = Frget training trials, FF = Frget-Frget training trials.
216 MILLER AND ARMUS The purpse f the tw-stimuli regular trials was t attempt t eliminate generalizatin decrement that might have resulted frm having regular trials with nly ne stimulus, but prbe trials with tw stimuli. Because sme f the regular trials cntained tw stimuli, and sme cntained nly ne, and this was als the situatin which was present in the prbe trials, generalizatin decrement shuld have been reduced r eliminated. Presentatin f the regular trials cntinued until the animals had reached a criterin f at least 65% crrect fr 4 ut f 5 cnsecutive days n at least ne f the tw types f remember trials. At this pint, prbe trials were intrduced, and data cllectin began. Type F Prbe Trials 0 Sample.Umul -------- F.u. S... delay '-_--'I,-I ---'I ::s. Reinfrcement N rejnfrcement Type F l. Prbe Trils Smple sum.l F cue S.. e delay.!l... Reue.. J! '"' Type R f Prbe Trial. Sampl limulu. Re S.. e delay F cue I I Cmparisn CmparilOn II II SUmull Stimuli Reinfrcement N reinfrcement N reidfrccmcat Reinfrcement Figure 2. Schematic representatin f prbe trials. F = Frget alne prbe trials, F R = Frget Remember prbe trials, and R F = Remember Frget prbe trials.
SHORT-TERM MEMORY OR CONDITIONED RESPONSE 217 Prbe trials. There were three types f prbe trials: 1. Type F: sample stimulus, F-cue, 5 s delay, cmparisn stimuli. 2. Type F-R: sample stimulus, F-cue, delay, R-cue, cmparisn stimuli. 3. Type R-F: sample stimulus, R-cue, delay, F-cue, cmparisn stimuli. (See Figure 2 fr a schematic representatin f the three different types f prbe trials.) These three types f prbe trials were presented alng with the fur types f regular trials fr a ttal f 180 trials per day fr 4 testing days. On each testing day, there were 30 R trials, 30 RR trials, 30 F trials, 30 FF trials, 20 F prbe trials, 20 F-R prbe trials, and 20 R-F prbe trials presented t each animal in randm rder. Percentage f crrect respnses n each f the three types f prbe trials and n the tw types f remember trials (R and RR) was the respnse measure. Results A 2 (R-cue type: bright, dim) x 4 (testing day) x 5 (prbe trial type: R, RR, F, F-R, R-F) mixed factrial ANOVA was used t analyze the data. The results shwed n main effects f either R-cue type r testing day, and n interactins invlving either f these tw factrs, s subsequent analyses were cllapsed acrss these variables. A ne-way within subjects ANOVA shwed a significant effect f prbe trial type, F(4, 32) = 5.105, P =.0027. Because the tw alternative hyptheses predict different patterns f results, it was necessary t cnduct planned cmparisns t determine where the differences lay. If the rehearsal hypthesis were crrect, then the percentage f crrect respnses in trial types F and F-R shuld have been significantly lwer than in trial types R, RR, and R-F, but nt different frm each ther. Als, n differences shuld have been fund amng percentage f crrect respnses in trial types R, RR, and R-F. If, in cntrast, the learned respnse r nnrespnse hypthesis were crrect, then the percentage f crrect respnses in trial types F and R-F shuld have been significantly lwer than in trial types R, RR, and F-R, but nt different frm each ther. These results are presented in Figure 3. Of the 10 planned cmparisns, the five differences that were significant were: 1. R> F-R, F(1, 8) = 7.189, P =.0115. 2. RR > F, F(1, 8) = 6.961, P =.0128. 3. RR > F-R, F(1, 8) = 14.692, P =.0006. 4. R-F> F, F(1, 8) = 4.907, P =.0340. 5. R-F> F-R, F(1, 8) = 11.627, P =.0018.
218 MILLER AND ARMUS 80 75 0 e If 0 U +l 70 65 c:: CD 0 If 60 55 50 R RR F F-R R-F Trial Type Figure 3. Percentage crrect n five types f trials. R = One-stimulus remember trial, RR = Tw-stimuli remember trial, F = Frget trial, F-R = Frget-Remember trial, and R-F = Remember-Frget trial. Bars indicate standard errrs. Discussin The results f this study wuld appear t supprt the directed frgetting hypthesis, rather than the learned respnse hypthesis. If the animals really had learned t ''frget'' the sample stimulus, as suggested by Maki and Hegvik (1980), then the additin f the R-cue fllwing the F-cue in the prbe trials shuld have had n effect. Perfrmance n prbe trial F-R shuld nt have been significantly different frm perfrmance n prbe trial F. This predictin was supprted. Perfrmance n prbe trial R-F shuld have been better than perfrmance n prbe trial F, because the animals received the R-cue, and had already rehearsed the material during the delay, s the additin f the F-cue immediately befre the presentatin f the cmparisn stimuli shuld nt have had an effect n the animals' perfrmance. This predictin was als supprted.
SHORT-TERM MEMORY OR CONDITIONED RESPONSE 219 If, hwever, the animals learned nly nt t respnd (rather than t ''frget''), then the additin f the R-cue n prbe trial F-R shuld have increased their level f perfrmance abve the level f perfrmance fund n prbe trial F. This predictin was nt supprted. Perfrmance n prbe trial R-F shuld nt have been significantly different frm perfrmance n prbe trial F, because in bth types f trials, the animals were presented with the "dn't respnd" cue. This predictin was als nt supprted. Hwever, there is sme ambiguity in the interpretatin f the results. Rather than the animals learning t rehearse r nt rehearse during training, they culd have been learning t attend t nly the first stimulus and t ignre the secnd stimulus. During the regular trial training, sme f the R-cue trials had ne stimulus, and sme had tw stimuli. Similarly, sme f the F-cue trials had ne stimulus and sme had tw stimuli. The prblem with this training methd was that the first stimulus predicted the presence r absence f the cmparisn stimuli at the end f the trial with 100% accuracy. The additin r nnadditin f a secnd stimulus was irrelevant; it prvided n additinal infrmatin abut whether the animal wuld have an pprtunity t chse between the cmparisn stimuli and pssibly receive reinfrcement at the end f the trial. Because f this, the animals may have learned t attend t the first stimulus and disregard the secnd. This wuld explain the btained results as well as the rehearsal hypthesis. Sme slight indicatin that this might have nt been the case, at least fr the secnd R-cue, might be deduced frm the failure t find a significant difference between trial types Rand F, but with a significant difference ccurring when trial type RR was cmpared t trial type F. The subjects perfrmed better than they did n F trials when a secnd R-cue was added, supprting the view that they did attend t the secnd R-cue. Hwever, because n difference was fund between the Rand the RR trials, it can nt be cnclusively established that the animals did attend t this secnd cue. Finally, it is pssible that, given the methd f training, the animals learned t use spatial cues in rder t remember the sample stimulus during the delay perid. This was pssible because the sample stimuli were munted abve the cmparisn stimuli. The animals, therefre, may have learned t simply wait near the light which had been n during the delay perid in rder t "remember" which lever t press, r t abandn their psitin near the lever during the delay perid after a "frget" cue. That the pattern f results in this experiment can be explained by spatial psitin, hwever, is nt relevant t the hypthesis put frth. The F-cue, in this case, des interfere with the rehearsal f the sample stimulus. The mechanism by which it interferes with rehearsal may be "frgetting" (a central mechanism), r it may be by abandning the spatial psitin (a peripheral mechanism). S, althugh the results f this experiment shw that the F-cue interferes with rehearsal, the mechanism by which this takes place is nt specified.
220 MILLER AND ARMUS References GRANT, D. S. (1981). Stimulus cntrl f infrmatin prcessing in pigen shrtterm memry. Learning and Mtivatin, 12, 19-39. LEITH, C. R., & MAKI, w. S., Jr. (1975). Attentin shifts during matching-tsample perfrmance in pigens. Animal Learning and Behavir, 3, 85-89. MAKI, W. S. (1979). Pigens' shrt-term memries fr surprising vs. expected reinfrcement and nnreinfrcement. Animal Learning and Behavir, 7, 31-37. MAKI, W. S., & HEGVIK, D. K. (1980). Directed frgetting in pigens. Animal Learning and Behavir, 8, 567-574. MAKI, W. S., OLSON, D., & REGO, S. (1981). Directed frgetting in pigens: Analysis f cue functins. Animal Learning and Behavir, 9,189-195. SANTI, A., & SAVICH, J. (1986). Directed frgetting effects in pigens: Remember cues initiate rehearsal. Animal Learning and Behavir, 13, 365-369. STONEBRAKER, T. B., RILLING, M., & KENDRICK, D. F. (1981). Time dependent effects f duble cuing in directed frgetting. Animal Learning and Behavir, 9, 385-394.