prolonged visual memory in macaques and man

8/12/2019 Prolonged Visual Memory in Macaques and Man

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N~urosduncr Vol. 5. pp. 1825 to 1831Pergamon Press Ltd1980rinted m Great Britain0 IBRO

PROLONGED VISUAL MEMORYIN MACAQUES AND MAN

W. H. OVERMAN,R and R. W. DOTYCenter for Brain Research, University of Rochester, Rochester, New York 14642,U.S.A.

Ah&met-In delayed matching to sample an object or image (the sample) s presented, removed, andafter a certain delay is presented again together with a second object. The task is to identify (match) heobject previously seen. When the same pair of objects is used repeatedly, one or the other serving assample,monkeys have difficulty making the match after a few seconds. The task has thus been used as atest of short-term memory. The present experiments show, however. &hat if a diiferent pair of images isuse for each trial, pigtailed macaques can make reliable matches 24-96 h after presentation of thesample; longer intervals have not been tested.

While the macaques were not as proficient as man in this regard, this may well be a matter oftechnique in asking them the question. In any event they possess a visual system capable of prolongedretention of detail without benefit of linguistic support or rehearsal.

MANS memory for visual images is unquestionablyremarkable, and appears to be essentially limitless(NICKERSON, 968; STANDING,CONEZIO HABER,1970; STANDING, 973). Memory for pictures is gener-ally superior to memory for linguistic material,whether recall or recognition is the measure of reten-tion, and whether the linguistic material is presentedaurally or visually (SHEPARD, 967; PAVIO,ROGERS&SMYTHE, 968; COHEN,1973; STANDING, 973).It remains uncertain, however, as to what degreepictorial memory is aided by linguistic encoding ofthe perceived material (YERKES NISSEN 1939: PAVIOet al. 1968; see COHEN,1973). It is thus important toknow whether visual memory in animals approachesthat in man. This is p~ticularly reievant for thehigher primates, in which the anatomy and basic psy-chophysical characteristics of the visual system arenearly identical with those of man (e.g., POLYAK,1957; Scot POWELL, 1963; BROU~N WALD,1963; MARKS, DOBEL LE MACNI CHOLL, 1964;COHEN,1965; DEVALOIS J ACOBS, 971; SHKOLNIK-YARROS,1971; CAVONI US ROBBINS, 973; DEVALOIS,MORGAN,POLSON,MEAD HULL, 1974; SARMIENTO,1975; PFARLMAN,BIRCH & MEAMIWS, 1979; B~LTZ,HARWERIH& SMITH, 1979; COWEY, 1979). In otherwords, is it possible that visual memory is somehowassociated with the anatomy and physiology of thevisual system, or does it require subs~nt~al supportfrom the uniquely human endowment of language?Rather surprisingly, this question has heretofore notbeen directly considered, although there are manyrelevant studies.The mnenomic capabilities of macaques, forinstance, are not in doubt, BERITASHVILI1972) havingreported their ability to remember where food waslast located even after a lapse of several months.

Present address: Department of Psychotogy, P.O. Box3725, University of North Carolina at Wilmington, Wilm-ington, NC 28401, U.S.A.

Memory for location, however, may be uniquelysuperior relative to other mnemonic categories, (e.g.MAC~ORQUO~ALE,947; see MI SHK IN DEL ACOUR,1975), and a test must thus be devised which assaysretention purely of visual cues. Such a test is availablein the procedure of delayed matching to sample, ori-ginated in its modern form in Harlows laboratory byWEINSTEIN 1941). A sample object or image is firstshown and removed. Then, after a certain interval,(the delay period), the sample is again showntogether with one or more other objects or imagesand the subject is required to identify the one seenoriginally. Weinstein showed that macaques and threeyear old children were comparable in their perform-ance on this task, using delays of 5, 10 and 1.5 ; oneof the children, however, failing to respond withdelays longer than 5 s. HAYES6% THOMPSON 1953),working with chimpanzees, used a new pair of stimulifor each trial, recognizing that if the same pair ofstimuli is used from one trial to the next, with thesample being first one and then the other of the pair,the problem becomes one of distinguishing the mostrecent from multiple past changes in significance.Despite this caveat that trial-unique stimuli arerequired to avoid confusion, not only of the animalsbeing tested but in the interpretation of the results,delayed matching to sample with a small number ofrepeatedly used stimuli became a rather popularmeans of testing short term memory in monkeys (e.g.SCHECKEL, 965; ETKIN & DAmro, 1969; JARVIK,GOLDFARB& CARLEY,1969; JARRAD& MOISE,1971;MELLO,1971; see MEDIN DAVI S, 1974; MISHK INDELACOUR,975). The procedure of HAYES THOMP-SON 1953) has gradually been rediscovered ( KINDAMATO, 1969; GAFFAN, 1974; MAXIN WILSON,1974; MI~HKIN DELACOUR, 975; WORSHAM, 975).

We have here examined whether trial-uniquestimuli are essential for monkeys to perform correctlywhen the delay between sample and matchingstimuli is more than a few seconds and if, when such a

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IX26 W. H. ~WXMAN. JK and R. W. Dot\

procedure is used, a monkeys visual memory clearlyexceeds the short term, and approaches that ofhuman subjects presented with the same material.

EXPERIMENTAL PROCEDURESSuhircr.~

Four male and two female adolescent macaques(Macnca rtrrnestrina) were tested. Two of them, labeledM51A and MSlC. learned and performed all of the tasksunder monocular viewing conditions because each had oneeye sutured closed since birth for participation in researchwhich was unrelated to the present study.Methods

The animals were trained in a sound reducing chamberwhich was equipped with a one-way observation window.Seated in a restraining chair which allowed free arm move-ment, the monkeys were positioned 25 cm in front of three

x 15 cm opalescent plastic rear projection panels whichwere horizontally aligned and separated by 2 cm betweeneach panel (Fig. 1). Three Kodak Carousel projectors.equipped with 180-mm lenses and extension tubes, pro-jected standard 35 mm color transparencies as fine resolu-tion, 5.5 x 7 cm images. One hundred different transparen-cies were used for most of the experiments and wereshuffled randomly each day to make SO pairs, the pairsthus differing from day to day, although the monkeys pre-sumably became familiar with each of the 100 stimuli beingused. For the most part, these transparencies (or slides)were of common human artifacts, e.g. a shoe, a screwdriver. spectacles. coffee mug, etc.

The monkey was requued to press the approprtatelilluminated panel to recetve a reward of orange Juice, delt-vered through a spout which did not impinge upon Its viewof the panels (Fig. I). For the initial training on each trialthroughout the session a different sample picture wa\ pro-tected on the center panel and the animal was requtred tomess it nine times for reinforcement. At the instant of re-inforcement thts center panel was extinguished concur-rcntly with illumination of both outside panels (Icro d&q).one showing the sample which the animal had Just rcs-ponded to and the other showing the compartson sttmulus.The crucial factor was the disappearance of the image fromthe center panel and its Immediate reappearance at one orthe other of the outside panels. i.e. the visual effect was asthough the sample stimulus had merely been dtsplacedlaterally.

The animals tended to respond to the stimulus that hadbeen reinforced, even though it had moved to a new pos-ition. This simultaneous offset-onset procedure overcamethe monkeys spontaneous preference for novel stimuhwhich, in a trial-unique paradigm. can result m a strongtendency to respond to the comparison stimulus (MISHKI~

DLLACOUK. 1975). In the present study one response(match) to the original sample stimulus resulted in re-inforcement. and extinction of the lateral panels. whereas aresponse to the comparison stimulus produced extinctionof the panels plus pumshment (puff of compressed air).

The first experiment tested the ammals abihty toremember familiar but trial-unique stimuli at retentionintervals from 5 s to 24 h (Fig. 2. condition 1).After learn-

1 - TRlAL UNIOLIE2 - NOVEL STIMULI

111 I 1 I I5 15 30 60 120 180 v- 241,~

DEL AY I\tc.iFIG. 2. Mean percent correct response for six macaques on a delayed-matching-to-sample task underfour stimulus conditions, as per the code, numbered corresponding to experiments (see ExperimentalProcedures). Note the great difference in accuracy of matching even at relatively brief delays for the useof trial unique stimuli versus repeated use of the same pair of stimuli (condition 4). Where it was possibleto do so without confusing the various curves, vertical lines indicate the range of individual scores. Therange of other values for 30, 60, and 180 s, 1 h and 24 h, respectively are: Condition 1, St&SO/,, 7688,,.60_8Oq& 51-604, SCrSOT< Condition 2, 84-100x, 7696x, 7492%, 47-87%, 54-SST,,, Condition 3,

82-92%. 84100;/& 64-88;, 40.87,,, 47767,


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Fro 1. pigtail macaque. performing a simultaneous match (left panel) to sample (center panel) in te-sponse to trial-unique stimuli, which are projected images. The animal is seated in a restraining chairwhich allows free arm movement. The white tube to the left of the monkeys head is the spout throughwhich orange juice is delivered as a reward for correct responses. In the normal course of the experi-ments the central and lateral panels were nexer illuminated concurrently, but are shown here merely for

illustrative purposes.

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Visual memory 1829ing the zero-delay task, the animals were taught to matchwith a delay interposed between the disappearance of thesample and its reappearance together with the comparison.In this paradigm the animals had 50 trials/day with fami-liar but trial-unique stimuli, eventually at each of he fol-lowing delay intervals: 5, 10, 15, 30, 60 and 180s. Fifteentrials each were given at I h and 24 h delay intervals.Transfer from the zero-delay task to the delayed match-ing task required no special training. Since 3 min proved tobe about the maximum time these adolescent monkeyswould sit quietly and remain attentive to the testing situ-ation, for the 1 hr delay they were removed from the testchamber after the sample presentation, returned to theirhome cage and then brought back 1 h later for the match-ing part of the trial. Five such 1 h delay trials were givenfor 3 consecutive days. The 24 h trials were administeredconcurrently with the tests at the shorter delay intervals.The animals were presented with a sample stimulus at theend of a days test session, returned to the home cage for24 h and, at the beginning of the following days session,were presented with the matching part of that trial. Thenthe usual block of trials at shorter delays was administered.Experiment 2

The second experiment tested the animals ability toremember stimuli which had never been seen before. Theanimals were tested at delays of 30, 60, 180 S, 1 and 24 hwith 180 completely novei stimuli which were used onlyonce as sample or comparison. Blocks of 25 trials wereused for the 30, 60, and 180s delays intermixed with 15trials using the familiar stimuli (Fig. 2, condition 2).Experiment 3

In order to control for the effects of practice, the thirdexperiment was a retest of experiment l-delayed match-ing with the original familiar stimuli, using delay intervatsof 30, 60, f 80 s, 1and 24 h (Fig. 2, condition 3).Experimeni I

In the fourth experiment at short delay intervals an in-variant pair of stimuli was usd, trial after trial, one beingthe sample and the other the comparison stimulus on arandom basis for any given trial, in blocks of 50 trials at 5,10, 15, and 30 s delays (Fig. 2, condition 4).Experiment 5

In this experiment monkey and human subjects werecompared on a 48 h retention test which was procedurallyanalogous to previous tests conducted with human subjects(STANDING et al. 1970; STANDING, 1973). Each of threemonkey and two human subjects were shown 25 successiveslides which they had never seen before. The monkeys wererequired to press each image nine times for orange juicereward and the human subjects were required to press theilluminated panel nine times without reward but withinstructions: look at the stimulus in anticipation OFa vis-ual memory task. Forty-eight hours later all subjects weregiven 25 two-choice discriminations between those imagespresented earlier and another 25 images which they hadnever seen before. The monkeys performed poorly on thistask (Fig. 3), but it was suspected this might be attributableto their failure to attend to the wholly unfamiliar imagesemployed.

In order to ensure that the subjects did, in fact, attend tothe sample stimuli, a procedure was devised to provide the

FIG. 3. Percent correct response for human and monkeysubjects in matching to sample after a delay of 48 h withstimuli that had been presented only once (novel) or 12times (familiar). Vertical lines represent the range of scoresand the horizontal broken line represents chanceperformance.monkeys, and three new human subjects, with a specifieddegree of familiarity with the test stimuli and, for the mon-keys, to associate the discriminated stimuli with reward. Tothis end another 50 images not previously seen were usedover a period of 4 days in such a manner that the 25images ultimately used had been viewed 12 times and, forthe monkeys, associated with reward (i.e., served as sam-ple) eight times in trials with a 5 s delay. After an intervalof 48 h since their last viewing, these 25 familiar imageswere then paired with a second set of 25 other imageswhich had never previously been seen (Fig. 3).

Both human subjects and monkeys participated in fourconsecutive days of 5 s delayed-matching-to-sample with50 slides which had never been seen. On day 1, 25 slideswere arbitrarily designated as samples and 25 comparisons.The subjects twice performed the 5 s delayed-mat~hing-to-sample with these slides; on the second sequence the out-side slide trays were reversed so that the correct matchwould appear on the stimulus panel opposite from the firstsequence. Thus, each sample slide was viewed four timeseach day (once as sample and once as correct match in twopresentations) while each comparison slide was seen twice(as comparison in two presentations). On day 2, the slideswhich had served on day I as samples were chosen as thecomparison stimuli and those which had been comparisonslides on day I were samples, the samples and comparisonsbeing randomly matched. As on day 1, the sequence waspresented twice. Thus, in two days each slide was seen sixtimes and, as samples, associated with reinforcement fourtimes. This procedure was followed for 4 days, hence eachslide was viewed 12 times and associated with reward eighttimes.

RESULTSRather than describe the results of each of the

above six experiments separately they will be com-pared, as set forth in Table 1 and Figs 2 and 3.The amount of training required for the six naivemacaques to achieve a level of 90% correct responsesfor two consecutive days on simultaneous matchingto sample, i.e., zero delay, is shown in Table 1. Themean was 14 f 3.5 days of training with a mean totalof 213 _+48.5 errors.


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1830 h. H. ()\I RMA\. JK ~tld R. w I)OII

TAULI- 1. TRIALS Axr) ERRORS To ~1 ARNIUC; CRITLRIOY FORSIX tXPl:RIMENTALLr NAVVY MACAQUES WE,~L~: L~ARNI~xG AMATCHriXG-TO-SAMPLt rASli WIT,, A L,.RO I)ELA\ Ttif.XOR~S ARt lNCLlJSl\t:Ot Itrt tW0 CONS~(,I Il\l. (R,Tt:R,OI\

SI.SSIONS OF I,, CORRI. r R~SPO~S, S.-~ .___.--.

Blocks ofSubject 50 trials ErrorsM 51C I I 153M 7-7 II IX2M 7-5 I 196M7-4 13 218M 51A 16 235M7 6 0 293

Most of the animals were then immediately able tomaintain this level of performance with delays up toI5 s (Fig. 2). With longer delays the performancebegan to deteriorate somewhat, although the two bestanimals maintained the 9004 correct level up to a 24 hdelay (Fig. 2, condition 2) when completely novelstimuli were used. Even for the group of six maca-ques, performance is significantly above chanceP 0.05)t 3 min (Fig. 2, condition 1). There is little

improvement consequent to increased experience(conditions 1 vs 3, Fig. 2). Individually the monkeyswere somewhat erratic in their performance, therebeing none which were consistently better or worsethan the group across all the delay intervals.

The increase in accuracy of matching at longerintervals, achieved with the use of novel stimuli(condition 2 in Fig. 2), was sufficiently variable fromone animal to another that it was not statisticallysignificant (U test comparison with condition 3-mFig. 2: P < 0.056 at 180s; P < 0.19 at 1 h; andP < 0.09 at 24 h).

The effect of using a single pair of stimuli over andover again, however, was dramatic and unequivocal(Fig. 2, condition 4). Under these conditions even thebest animals performed at little better than chancelevels after a delay of only 30 s.

Despite their excellent performance after a delay of24 h when completely novel stimuli were used, themonkeys attained only chance levels under theseconditions after 48 h (Fig. 3). This is probablyattributable to an error in experimental design. The25 novel sample stimuli were simply presentedseriatim, with the monkey pressing each nine times toreceive its reward of fruit juice. Thus, no demand wasmade upon the monkey to attend to the sample toreceive its reward, and the results certainly suggestthat they ignored the stimuli and simply pressed thepanel. When stimuli were used which had been clearlyassociated with reward, their selections were 76-86x,correct after this 2 day interval (Fig. 3). Selection bythe human subjects in both situations was virtuallyerrorless.

For a single monkey the f:mlthar $timuh WCICusedagain to give 25 trials iit XII lnter\al of Yh II. Thecorrect match was made on 19of these trials. i.~.. 7h,,correct.

The results show unequivocally that macaques canstill recognize purely pictorial material man) hours(days) after its initial presentation. Visual memory isthus remarkably accurate even in the absence of anpossibility of verbal encoding or rehearsal. A similarconclusion can be drawn from the experiments oiGAFFAN (1977). in which macaques could stillrecognize a picture as having been previously seenthat day even though it followed presentation of asmany as 18 others pictures to which the monkeymight or might not have to respond.

The clear human superiority at such tasks (Fig. 3)may be in part attributable to linguisticcategorization. However. it is more likely that thedifference here between monkcq and man hes inshortcomings of the techniques employed to get themonkey to pay attention to the sample stimuli. Thisdifficulty has long plagued research of this type;TINKELPAUGH (1932). YEKKES & NISSEN (1939). andHAYES & THOMPXIN 1953) all having reported ratherpoor performances even of chimpanzees, whileremarking on the animals frequent inattentiveness.Such an effect is undoubtedly present in Fig. 3 at 48 hfor the novel stimuli, which shows such a strikingcontrast with the use of novel stimuli in Fig. 2 at 24 h;the former having been presented in a context wherethe monkey was not motivated to attend to them.

The results also confirm WI:ISKKAKTZS suspicions(1970) concerning the fallibility of measures of shortterm memory. The animals which seem to retain thevisual image for only a few seconds when the samepair of stimuli is used rcpcatedly (Fig. 2), can retrievethese stimuli with a high degree of accuracy even after24 h if they are used but once per day (Fig. 2). Ratherthan being a problem of short term memory in theformer case, it seems apparent that the animal, asindeed also does its human observer, merel , hasdifficulty dissociating the momentary significance ofthe monotonously recurring stimuli from theirmultiple past changes in significance. Short termmemory may exist. but the paradigm of delayedmatching to sample 1s not an appropriate way tomeasure or identify it..Ickrlowlrdyemc,nts This work was \upported by (irantNS 03606 from the National lnstltute of Neurological andCommunicative Disorders and Stroke. National lnstltutcsof Health. We are indebted to the late J. R. BARTUI I forhis patient assistance with the electronic control circtntr\ i.and to R. A. SLOANP for help in tratnlng home 01 theanimals.


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prolonged visual memory in macaques and man

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