N~urosduncr Vol. 5. pp.

1825 to 1831 Pergamon Press Printed m Great Britain 0 IBRO

Ltd1980

PROLONGED VISUAL MEMORY IN MACAQUES AND MAN

W. H. OVERMAN, JR and R. W. DOTY Center for Brain Research, University of Rochester, Rochester, New York 14642,U.S.A. delayed matching to sample an object or image (the sample)is presented, removed, and after a certain delay is presented again together with a second object. The task is to identify (match)the object previously seen. When the same pair of objects is used repeatedly, one or the other serving as sample,monkeys have difficulty making the match after a few seconds. The task has thus been used as a
Ah&met-In test of short-term memory. The present experiments show, however. &hat if a diiferent pair of images is used for each trial, pigtailed macaques can make reliable matches 24-96 h after presentation of the sample; longer intervals have not been tested. While the macaques were not as proficient as man in this regard, this may well be a matter of technique in asking them the question. In any event they possess a visual system capable of prolonged retention of detail without benefit of linguistic support or rehearsal.

in the procedure of delayed matching to sample, originated in its modern form in Harlows laboratory by WEINSTEIN (1941). A sample object or image is first shown and removed. Then, after a certain interval, (the delay period), the sample is again shown together with one or more other objects or images and the subject is required to identify the one seen originally. Weinstein showed that macaques and three year old children were comparable in their performance on this task, using delays of 5, 10 and 1.5s; one of the children, however, failing to respond with delays longer than 5 s. HAYES6% THOMPSON (1953), working with chimpanzees, used a new pair of stimuli 1957; Scot & POWELL, 1963; BROU~N & WALD, for each trial, recognizing that if the same pair of 1963; MARKS, DOBELLE& MACNICHOLL, 1964; stimuli is used from one trial to the next, with the COHEN,1965; DEVALOIS & JACOBS, 1971; SHKOLNIK- sample being first one and then the other of the pair, YARROS, 1971; CAVONIUS & ROBBINS, 1973; DEVALOIS, the problem becomes one of distinguishing the most MORGAN,POLSON, MEAD & HULL, 1974; SARMIENTO, recent from multiple past changes in significance. 1975; PFARLMAN, BIRCH & MEAMIWS, 1979; B~LTZ, Despite this caveat that trial-unique stimuli are HARWERIH& SMITH, 1979; COWEY, 1979). In other required to avoid confusion, not only of the animals words, is it possible that visual memory is somehow being tested but in the interpretation of the results, associated with the anatomy and physiology of the delayed matching to sample with a small number of visual system, or does it require subs~nt~al support repeatedly used stimuli became a rather popular from the uniquely human endowment of language? means of testing short term memory in monkeys (e.g. Rather surprisingly, this question has heretofore not SCHECKEL, 1965; ETKIN & DAmro, 1969; JARVIK, been directly considered, although there are many GOLDFARB & CARLEY,1969; JARRAD& MOISE,1971; relevant studies. MELLO,1971; see MEDIN& DAVIS, 1974; MISHKIN & The mnenomic capabilities of macaques, for DELACOUR, 1975). The procedure of HAYES & THOMPinstance, are not in doubt, BERITASHVILI (1972) having SON(1953) has gradually been rediscovered (&KIN & reported their ability to remember where food was DAMATO, 1969; GAFFAN, 1974; MAXIN & WILSON,
last located even after a lapse of several months. 1974; MI~HKIN & DELACOUR, 1975; WORSHAM, 1975). We have here examined whether trial-unique

MANS memory for visual images is unquestionably remarkable, and appears to be essentially limitless (NICKERSON, 1968; STANDING,CONEZIO& HABER, 1970; STANDING, 1973). Memory for pictures is generally superior to memory for linguistic material, whether recall or recognition is the measure of retention, and whether the linguistic material is presented aurally or visually (SHEPARD, 1967; PAVIO,ROGERS & SMYTHE, 1968; COHEN,1973; STANDING, 1973). It remains uncertain, however, as to what degree pictorial memory is aided by linguistic encoding of the perceived material (YERKES & NISSEN, 1939: PAVIO et al., 1968; see COHEN,1973). It is thus important to know whether visual memory in animals approaches that in man. This is p~ticularly reievant for the higher primates, in which the anatomy and basic psychophysical characteristics of the visual system are nearly identical with those of man (e.g., POLYAK,

Memory for location, however, may be uniquely superior relative to other mnemonic categories, (e.g. MAC~ORQUO~ALE, 1947; see MISHKIN & DELACOUR, 1975), and a test must thus be devised which assays retention purely of visual cues. Such a test is available

Present address: Department of Psychotogy, P.O. Box 3725, University of North Carolina at Wilmington, Wilmington, NC 28401, U.S.A.

stimuli are essential for monkeys to perform correctly when the delay between sample and matching stimuli is more than a few seconds and if, when such a
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IX26

W. H.

~WXMAN.

JK and R. W. Dot\ The monkey was requued to press the approprtatel! illuminated panel to recetve a reward of orange Juice, deltvered through a spout which did not impinge upon Its view of the panels (Fig. I). For the initial training on each trial throughout the session a different sample picture wa\ protected on the center panel and the animal was requtred to mess it nine times for reinforcement. At the instant of reinforcement thts center panel was extinguished concurrcntly with illumination of both outside panels (Icro d&q). one showing the sample which the animal had Just rcsponded to and the other showing the compartson sttmulus. The crucial factor was the disappearance of the image from the center panel and its Immediate reappearance at one or the other of the outside panels. i.e. the visual effect was as though the sample stimulus had merely been dtsplaced laterally. The animals tended to respond to the stimulus that had been reinforced, even though it had moved to a new position. This simultaneous offset-onset procedure overcame the monkeys spontaneous preference for novel stimuh which, in a trial-unique paradigm. can result m a strong tendency to respond to the comparison stimulus (MISHKI~ & DLLACOUK. 1975). In the present study one response (match) to the original sample stimulus resulted in reinforcement. and extinction of the lateral panels. whereas a response to the comparison stimulus produced extinction of the panels plus pumshment (puff of compressed air).

procedure is used, a monkeys visual memory clearly exceeds the short term, and approaches that of human subjects presented with the same material.
EXPERIMENTAL Suhircr.~ Four male and two female adolescent macaques (Macnca rtrrnestrina) were tested. Two of them, labeled M51A and MSlC. learned and performed all of the tasks under monocular viewing conditions because each had one eye sutured closed since birth for participation in research which was unrelated to the present study.
Methods

PROCEDURES

The animals were trained in a sound reducing chamber which was equipped with a one-way observation window. Seated in a restraining chair which allowed free arm movement, the monkeys were positioned 25 cm in front of three 9 x 15 cm opalescent plastic rear projection panels which were horizontally aligned and separated by 2 cm between each panel (Fig. 1). Three Kodak Carousel projectors. equipped with 180-mm lenses and extension tubes, projected standard 35 mm color transparencies as fine resolution, 5.5 x 7 cm images. One hundred different transparencies were used for most of the experiments and were shuffled randomly each day to make SO pairs, the pairs thus differing from day to day, although the monkeys presumably became familiar with each of the 100 stimuli being used. For the most part, these transparencies (or slides) were of common human artifacts, e.g. a shoe, a screw driver. spectacles. coffee mug, etc.

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

1 2 -

TRlAL NOVEL

UNIOLIE STIMULI

111 5 15

I 30

1 60

I 120 DEL

I 180 AY I\tc.i v241,~

FIG. 2. Mean percent correct response for six macaques on a delayed-matching-to-sample task under four stimulus conditions, as per the code, numbered corresponding to experiments (see Experimental Procedures). Note the great difference in accuracy of matching even at relatively brief delays for the use of trial unique stimuli versus repeated use of the same pair of stimuli (condition 4). Where it was possible to do so without confusing the various curves, vertical lines indicate the range of individual scores. The range 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,

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

1827

Visual memory ing the zero-delay task, the animals were taught to match with a delay interposed between the disappearance of the sample and its reappearance together with the comparison. In this paradigm the animals had 50 trials/day with familiar but trial-unique stimuli, eventually at each of the following delay intervals: 5, 10, 15, 30, 60 and 180s. Fifteen trials each were given at I h and 24 h delay intervals. Transfer from the zero-delay task to the delayed matching task required no special training. Since 3 min proved to be about the maximum time these adolescent monkeys would sit quietly and remain attentive to the testing situation, for the 1 hr delay they were removed from the test chamber after the sample presentation, returned to their home cage and then brought back 1 h later for the matching part of the trial. Five such 1 h delay trials were given for 3 consecutive days. The 24 h trials were administered concurrently with the tests at the shorter delay intervals. The animals were presented with a sample stimulus at the end of a days test session, returned to the home cage for 24 h and, at the beginning of the following days session, were presented with the matching part of that trial. Then the usual block of trials at shorter delays was administered.
Experiment 2

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FIG. 3. Percent correct response for human and monkey subjects in matching to sample after a delay of 48 h with stimuli that had been presented only once (novel) or 12 times (familiar). Vertical lines represent the range of scores and the horizontal broken line represents chance performance. monkeys, and three new human subjects, with a specified degree of familiarity with the test stimuli and, for the monkeys, to associate the discriminated stimuli with reward. To this end another 50 images not previously seen were used over a period of 4 days in such a manner that the 25 images ultimately used had been viewed 12 times and, for the monkeys, associated with reward (i.e., served as sample) eight times in trials with a 5 s delay. After an interval of 48 h since their last viewing, these 25 familiar images were then paired with a second set of 25 other images which had never previously been seen (Fig. 3). Both human subjects and monkeys participated in four consecutive days of 5 s delayed-matching-to-sample with 50 slides which had never been seen. On day 1, 25 slides were arbitrarily designated as samples and 25 comparisons. The subjects twice performed the 5 s delayed-mat~hing-tosample with these slides; on the second sequence the outside slide trays were reversed so that the correct match would appear on the stimulus panel opposite from the first sequence. Thus, each sample slide was viewed four times each day (once as sample and once as correct match in two presentations) while each comparison slide was seen twice (as comparison in two presentations). On day 2, the slides which had served on day I as samples were chosen as the comparison stimuli and those which had been comparison slides on day I were samples, the samples and comparisons being randomly matched. As on day 1, the sequence was presented twice. Thus, in two days each slide was seen six times and, as samples, associated with reinforcement four times. This procedure was followed for 4 days, hence each slide was viewed 12 times and associated with reward eight times. RESULTS

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

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

In the fourth experiment at short delay intervals an invariant pair of stimuli was usd, trial after trial, one being the sample and the other the comparison stimulus on a random 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 were compared on a 48 h retention test which was procedurally analogous to previous tests conducted with human subjects (STANDING et al., 1970; STANDING, 1973). Each of three monkey and two human subjects were shown 25 successive slides which they had never seen before. The monkeys were required to press each image nine times for orange juice reward and the human subjects were required to press the illuminated panel nine times without reward but with instructions: look at the stimulus in anticipation OFa visual memory task. Forty-eight hours later all subjects were given 25 two-choice discriminations between those images presented earlier and another 25 images which they had never seen before. The monkeys performed poorly on this task (Fig. 3), but it was suspected this might be attributable to their failure to attend to the wholly unfamiliar images employed.

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

Rather than describe the results of each of the above six experiments separately they will be compared, as set forth in Table 1 and Figs 2 and 3. The amount of training required for the six naive macaques to achieve a level of 90% correct responses for two consecutive days on simultaneous matching to sample, i.e., zero delay, is shown in Table 1. The mean was 14 f 3.5 days of training with a mean total of 213 _+48.5 errors.

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TAULI-

h. H. ()\I

RMA\.

JK ~tld R. w

I)OII

1. TRIALS

Axr) ERRORS To ~1 ARNIUC;

NAVVY MACAQUES

CRITLRIOY

FOR A

SIX tXPl:RIMENTALLr

WE,~L~: L~ARNI~xG

MATCHriXG-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~SPO~S, -~

S.

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

.___.--.

Subject M 51C M 7-7 M 7-5 M7-4 M 51A M7 6

Blocks of 50 trials

Errors

II
II I 13 16 0

153
IX2 196 218 235 293

Most of the animals were then immediately able to maintain this level of performance with delays up to I5 s (Fig. 2). With longer delays the performance began to deteriorate somewhat, although the two best animals maintained the 9004 correct level up to a 24 h delay (Fig. 2, condition 2) when completely novel stimuli were used. Even for the group of six macaques, performance is significantly above chance (P< 0.05) at 3 min (Fig. 2, condition 1). There is little improvement consequent to increased experience (conditions 1 vs 3, Fig. 2). Individually the monkeys were somewhat erratic in their performance, there being none which were consistently better or worse than the group across all the delay intervals. The increase in accuracy of matching at longer intervals, achieved with the use of novel stimuli (condition 2 in Fig. 2), was sufficiently variable from one animal to another that it was not statistically significant (U test comparison with condition 3-m Fig. 2: P < 0.056 at 180s; P < 0.19 at 1 h; and P < 0.09 at 24 h). The effect of using a single pair of stimuli over and over again, however, was dramatic and unequivocal (Fig. 2, condition 4). Under these conditions even the best animals performed at little better than chance levels after a delay of only 30 s. Despite their excellent performance after a delay of 24 h when completely novel stimuli were used, the monkeys attained only chance levels under these conditions after 48 h (Fig. 3). This is probably attributable to an error in experimental design. The 25 novel sample stimuli were simply presented seriatim, with the monkey pressing each nine times to receive its reward of fruit juice. Thus, no demand was made upon the monkey to attend to the sample to receive its reward, and the results certainly suggest that they ignored the stimuli and simply pressed the panel. When stimuli were used which had been clearly associated with reward, their selections were 76-86x, correct after this 2 day interval (Fig. 3). Selection by the human subjects in both situations was virtually errorless.

The results show unequivocally that macaques can still recognize purely pictorial material man) hours (days) after its initial presentation. Visual memory is thus remarkably accurate even in the absence of an! possibility of verbal encoding or rehearsal. A similar conclusion can be drawn from the experiments oi GAFFAN (1977). in which macaques could still recognize a picture as having been previously seen that day even though it followed presentation of as many as 18 others pictures to which the monkey might or might not have to respond. The clear human superiority at such tasks (Fig. 3) may be in part attributable to linguistic categorization. However. it is more likely that the difference here between monkcq and man hes in shortcomings of the techniques employed to get the monkey to pay attention to the sample stimuli. This difficulty has long plagued research of this type; TINKELPAUGH (1932). YEKKES & NISSEN (1939). and HAYES & THOMPXIN (1953) all having reported rather poor performances even of chimpanzees, while remarking on the animals frequent inattentiveness. Such an effect is undoubtedly present in Fig. 3 at 48 h for the novel stimuli, which shows such a striking contrast with the use of novel stimuli in Fig. 2 at 24 h; the former having been presented in a context where the monkey was not motivated to attend to them. The results also confirm WI:ISKKAKTZS suspicions (1970) concerning the fallibility of measures of short term memory. The animals which seem to retain the visual image for only a few seconds when the same pair of stimuli is used rcpcatedly (Fig. 2), can retrieve these stimuli with a high degree of accuracy even after 24 h if they are used but once per day (Fig. 2). Rather than being a problem of short term memory in the former case, it seems apparent that the animal, as indeed also does its human observer, merel!, has difficulty dissociating the momentary significance of the monotonously recurring stimuli from their multiple past changes in significance. Short term memory may exist. but the paradigm of delayed matching to sample 1s not an appropriate way to measure or identify it.
.Ickrlowlrdyemc,nts
NS 03606 from Communicative of Health. his patient and to animals. This Disorders with work was \upported National control by (irant and

the National

lnstltute and Stroke.

of Neurological

lnstltutcs

We are indebted assistance R. A. SLOANP for

to the late J. R. BARTUI the electronic help in tratnlng home

for

circtntr\i. 01 the

Visual memory REFERENCES

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