Hemispheric differences in memory search

Neuropsycholog,a, Vol 18, pp. 665 to 673 “8 Pergamon Press Ltd.. 1980. Prmted m Great Bnlam

HEMISPHERIC

DIFFERENCES

IN MEMORY

DAVID J. MADDEN and ROBERT

SEARCH

D. NEBES

Center for the Study of Aging and Human Development, Box 2980, Duke University Medical Center, Durham, NC 27710, U.S.A. (Rcceipcd

26 June 1980)

Abstract-Recent evidence suggests that memory demands contribute to visual field (VF) differences in tachistoscopic recognition. The present experiment examined VF differences in a memory-search paradigm using verbal stimuli (digits). The results demonstrated a significant advantage to right VF left hemisphere presentation that was associated with the memory comparison stage of the task, but not with the perceptual encoding and response stages. These data are more consistent with a relative efficiency model of hemispheric specialization than with a functional localization model.

VISUAL field (VF) differences in tachistoscopic recognition have been found to be an informative index of hemispheric specialization in normal humans (for reviews see [ 1,2]). While it has been traditionally assumed that VF differences in tachistoscopic tasks reflect the processes involved in visual perception (e.g. [3]), such tasks usually include some demands on retention as well. When these memory requirements have been investigated independently, they have been found to contribute to the VF differences obtained. For example, when a sequence of bilateral pairs of letters or digits is to be recalled on each trial, a right VF advantage in the accuracy of report is greater for items presented earlier in the sequence [4-61. HANNAY and MALONE [7] reported that (for their male subjects) a significant right VF advantage in trigram recognition was only present when there was a 5 or 10 set delay between trigram pairs and not when there was a 0 set delay. Using a delayedcomparison task with nonverbal stimuli (faces), MOSCWITCH et (II. [IS] found that a reactiontime (RT) advantage to left VF presentation only emerged when the representation of the first stimulus in iconic memory was no longer available. M~SCWITCH [l] even claims that the processing advantage of either the left or the right hemisphere is only apparent when “higher order” analyses (i.e. those leading to a relatively stable memory trace) are involved. One paradigm that is potentially useful for investigating the relationship between hemispheric specialization and memory is the memory-search task devised by STERNBERG [9]. In this paradigm subjects hold a varying number of items in memory and on each trial must decide whether or not a single visually presented recognition-probe item is a member of the memory set. Considerable evidence [lo] suggests that performance in this task is composed of a series of stages: encoding the probe, comparing the probe against the items in the memory set, yes/no decision, and response production. Decision RT in this paradigm is typically an increasing linear function of memory-set size (M) for both “yes” and “no” responses. The slope of the linear RT function can be considered an estimate of the duration of the comparison stage (i.e. the rate of memory search), since the slope is the average increase in decision time for each additional member of the memory set. Similarly, the intercept of this line is an estimate of the decision RT at M = 0,and thus the intercept represents the combined 665

666

DAVID J. MADDEN and ROBERT D. NEBES

duration of the encoding, decision, and response processes that are distinct from memory comparison. While various models have been developed of the nature of the memory search involved in this paradigm (e.g. [l l--l 3]), there is substantial agreement that the slope and intercept measures represent the durations of different processing stages. The advantage of the memory-search paradigm in the present context is that it provides a means of establishing the processing stage, within a particular decision task, at which hemispheric differences emerge. In addition, this stage analysis can help distinguish “strict localization” from “relative efficiency” models of hemispheric specialization of cognitive function in normal humans. That is, as MOXOVITCH 114, p. 611 notes, if only the left hemisphere contributes to the performance of the memory-search task (when verbal processing is involved) then a strict localization-of-function model would predict an RT advantage to right VF presentation that is constant over M. This RT advantage would be evident as a lower intercept of the RT function for the right VF probes and would represent the time required for the transfer ofthe probe representation from the right hemisphere to the left during the encoding stage. MCWOVIX-H’S 114, 151 model of “functional localization”, which proposes that in normal individuals any linguistic functions represented by the right hemisphere will be suppressed by the speech-dominant left hemisphere. would also predict a right VF advantage that is constant over M. If. however, both hemispheres contribute to the memory search. but the left hemisphere is just relatively more efficient, then the advantage of right VF presentation should increase over M as the number of required comparisons increases. This latter situation would be reflected in a lower slope value for the right VF probes, and the difference in slope between the VFs would be an estimate of the difference in the duration of the comparison stages for the two hemispheres. KLATZKY [ 163 and KLATZKY and ATKINSON [I73 have reported VF effects in the memorysearch paradigm. In KLATZKY’S 1161 experiment, subjects were given a memory set of two to five letters on each trial; the probe was either a letter, or a picture of an object whose name could begin with one of the letters in the memory set. The probe stimuli were presented unilaterally to the left and right VFs. Klatzky found that the intercept of the RT function was relatively lower for the left-hemisphere presentation of picture probes and for the righthemisphere presentation of letter probes. She interpreted these intercept differences in terms of the nature of the encoding required by the two types of stimuli. The picture probes required naming, and thus picture stimuli presented to the right hemisphere required transfer to the left hemisphere (for verbal encoding) before the comparison stage could be carried out. It was claimed that the comparison of the letter probes, however, could be carried out purely on the basis of their spatial configuration. The transfer to the right hemisphere for spatial encoding in this case would result in a larger intercept for probe letters presented to the left hemisphere. KLATZKY and ATKINSON [17] obtained similar VF differences in intercept values when the picture and letter probes were presented in a blocked rather than in a randomized manner. The results of Klatzky and Atkinson suggest that hemispheric differences in memory search are associated with the encoding of the probe rather than with the comparison stage; these results additionally support a strict localization model of hemispheric specialization. However. there are problems with the Klatzky and Atkinson findings that weaken these conclusions. KLATZKY 1161, for example, also mentioned that the slope of the RT function was lower for the right-hemisphere presentation of the picture probes, and this aspect of her data supports a relative efficiency model. In addition, only female subjects were run in [16] and [17], and previous studies have found that females demonstrate VF differences that are smaller in magnitude than those of male subjects [7, IS]. Finally, subjects in 1161 and [17]

HEMISPHERIC

DIFFERENCES

IN MEMORY

667

were not required to rely on the visual features of the letter stimuli, and VF differences in tasks involving the comparison of letters in memory have been observed to vary according to the decision strategy (e.g. “pictorial” or “linguistic”) used by the subject [14]. Both subject selection and stimulus selection may thus have contributed to Klatzky and Atkinson’s failure to obtain significant hemispheric differences for the memory comparison stage of their task when the probe stimuli were letters. Since laterality effects in the memory-search paradigm have important consequences for models of hemispheric specialization of function, the present experiment investigated VF differences for both male and female subjects in a memory-search task. The present stimuli were digits, which have been found to be sensitive to factors affecting the encoding stage [19], and for which an advantage in RT to right VF presentation has been reliably observed 1201. In view of the effects of serial position and retention interval noted above, it was expected that an advantage to right VF presentation would be more pronounced for the search through short-term memory represented by the slope values than for the encoding and response processes represented by the intercept values. METHOD Thirty-two ttght-handed Duke University undergraduates (16 M. 16 F. mean age= 20.0 yr) receivedeither course credit or a cash payment for participating in the present experiment. Subjects were screened for corrected visual acuity with a Bausch and Lomb Ortho-Rater and were required to have a rating of at least eight points (corresponding to 20/25 Snellen) on the near acuity scale for each eye, with a difference of no more than two pomts between eyes. The data of two additional subjects, whose error rate exceeded lo”,, of the trials, were excluded from the analysis.

On each trtal, the subjects’task was to decide whether or not a single visually-presented probe digit was a member of a previously memorized list. The probes were presented vta a Scientific Prototype three-channel tachistoscope. in w’lich the luminance level was set at 16 fL. The stimuli were black digits (Chartpack 72 pt Zentak Grotesk) mounted on white tachistoscope cards; each digit was approximately 0.75’ wide by I’ high at a viewing distance of91.4 cm. The midpoint of each digit was positioned 2’ either to the left or the right of the midpoint of the card. Subjects viewed the stimuli binocularly, and the exposure duration ofeach probe was 150 msec. Subjects indicated their dectstons by moving a hand-held paddle switch mounted in the middle of a board in front of the tachistoscope. Movement of the switch from a central position stopped a digital clock that had begun running at the onset of the probe. Half of the subjects (8 M, 8 F) always used their right hand to move the switch, and half used their left hand. Within each handgroup, half of the subjects moved the switch toward themselves for a ‘yes” decision and away from themselves for “no”. while the rest had the reverse arrangement. Subjects were tested individually in a single experimental session of approximately 1 hr. Two lists of experimental trials were constructed. each of which contained one block of trials for each of three memory-set sizes (hl=2. 3 and 4). A “fixed set” procedure was used in which subjects held the same two. three. or four digits in memory during each trial block. Digits were randomly assigned as memory-set Items with the constraints (1) that digits could not be repeated within a memory set and (2) that there be no digits m common between the corresponding two sets of a given stre for the two experimental lists. Each subject received both lists of trtals, and the order of presentation of the two lists was counterbalanced wtthin each hand-group. The order of pt.ccentation of the three blocks of test trials within a list was arranged so that, across both lists, each of the six posstble sequences of the three values of ,%Iwas given once in each half of the testmg session, for each hand-group. At the start of the testing session subjects read written instructions and were told to respond as rapidly as possible while still being correct. One practtce block of 24 trials, with a memory set of three digits, was given. Before each block of test trials subjects were shown the appropriate memory set in the tachistoscope and permitted to view it as long as they wished. Each experimental block contained 54 trials: six practtce trials followed by 48 test trutls. Each block contained 12 positive and 12 negattre test trials for each visual field. randomly ordered, wtth the constraint that a particular visual field not receive more than three trials in successton. On the positive trials, each digits in a particular memory set appeared I2 times as a probe for M= 2, 8 times for M=3, 6 times for ,CI=4, and the appearances ofeach digit were equally divided between the two visual fields. On the negative trials, the digits not in the memory set were selected and balanced over visual field as equally as possible. Each trial consisted of the

DAVID J. MADDEN and R~LEKI D. NEBES

668

following sequence of events: (1) the experimenter advancing a fixation dot for 1 xc; (3) the exposure of the probe digit for 150 stimulus card changer provided an audible signal of the initiation offset of the probe was immediately followed by the appearance until the onset of the next fixation dot.

new stimulus card; (2) the appearance of a central msec, and the subject’s response. The motor of the of a new trial. In order to prevent after-images. the of a visual noise mask that remained on the screen

RESULTS time A mean RT was obtained for each subject in each experimental condition. This mean was based on 24 trials, 12 from each list. In order to reduce variability in the RT distribution. individual trials that exceeded 1200 msec were discarded and not replaced. Less than 0.25 x, of the total trials were discarded for this reason. Trials on which an incorrect decision was made were also excluded from the RT analysis; error rates are reported below. Repeated measures ANOVAs were performed on the mean correct RTs, which demonstrated that (for both positive and negative trials) there was a significant (P
HEMISPHERIC

DIFFERENCES

IN MEMORY

NO

YES

650 l l_vF

y=456+3l.Eix

oRVF

y=475+21.5x

.

LVF

y=520+26.9x

o RvF

y=506+32.2x

I 2

I

l

450

669

I 2

I

I 4

I 4

FIG;. I. Mean reactjon time (RT) as a function of memory-set sue (M) and visual field of the prohe, with best-litting linear equations. averaged over response hand and sex of subject. The positive and negative trials are graphed separately.

Table I. Mean percentage error rate for each trial type. as a function of memory-set sire 1.21) and visual field of the probe. averaged over responx hand and xx of subject

Trial

type Negative ,I1

Pwtlve >%I V~hual

field

2

3

4

Left

I.95

1.30

2.34

Right

!.30

1.X’

I.17

2

I .A3 I .69

3

4

1.17 I.‘)5

I.04 I.82

positive trials) for probe digits presented to the right VF cleft hemisphere than for those presented to the left VF -right hemisphere. This finding suggests that hemispheric differences in the present version of the memory-search paradigm are associated with the comparison between the recognition probe and memory-set items, rather than with the identification of the probe and initiation of a response. Since the intercept of the RT function in the memorysearch task represents a mixture of the encoding, decision. and response stages, it is possible that VF differences for one of these stages do exist in the present paradigm, but are masked by variability associated with the other stages. A more sensitive test of hemispheric differences at the encoding stage. for example. would involve the manipulation of the perceptual clarity (i.e. clear vs degraded) of the recognition probe. Using just this approach, HELLICE [21] has recently found that, in a memory-search paradigm with letter stimuli, reducing the perceptual clarity of the probe leads to a left VF advantage for the intercept value and to a right VF advantage for the slope value. In the present experiment there was a nonsignificant tendency, on the positive trials, for the left VF intercept to be lower than the right VF intercept, which is consistent with Hellige’s pattern of results.

670

DAVIS J. MADDEN and ROBEKT D. NEBES

The present VF effect for the slope values is consistent with other reports that verbal memory demands contribute to the right VF advantage [4-73; it also supports MOSCOVITCH’S[l] claim that hemispheric differences are primarily a product of “later” stages of information processing. However, since the significantly lower slope for right VF presentation corresponds to a right VF advantage that increases over M (see Fig. l), the present results do not support MOSCOVITCH’S[14, 151 functional localization model. In the present paradigm, both hemispheres are apparently involved in the comparison stage, but the left hemisphere is relatively more efficient in the comparison process.* DAY’S [23,24] recent work with a lexical decision task also indicates that in normal individuals the right hemisphere does contribute to verbal performance. The present results differ from those of Klatzky and Atkinson in two respects. First, the VF differences obtained in [16] and [17] did not interact with decision type. In the present experiment, however, the right VF advantage for the slope values was restricted to the positive trials; no significant VF effects were present for the negative trials. This pattern has appeared in previous RT studies of VF effects ([25-271, [14, Experiments 1 & 3]), but the reason these two trial types tend to produce different results is not clear. HELLIGE [26] suggests that a bias towards a negative response occurs with peripheral presentation; if RT on the negative trials is more likely to represent a guess based on insufficient information, then any hemispheric specialization for a particular decision process would be less apparent on these trials. MOSCOVITCH [14], on the other hand, speculates that “different” (or “no”) decisions may involve the analysis of more features of the test stimulus than “same” (or “yes”) decisions. The negative-trial RT would thus represent the combined analyses of both hemispheres rather than the processing associated with either hemisphere individually. The second discrepancy with the earlier studies is that the present VF differences were associated with the slope values rather than with the intercept values. The fact that Klatzky and Atkinson only used female subjects is apparently not responsible for this discrepancy, since no main effect or interaction involving sex of subject was significant in the present data analyses. One possible reason for the different results across studies is the difference in stimuli used. Long-term memory contains a variety of information about each letter of the alphabet (e.g. its alternative case forms, rhyming letters, vowel/consonant assignment), and as noted earlier, the VF differences associated with the delayed recognition of letters depend on the type of decision strategy being used. When a particular strategy is not required, digits may show a more consistent right VF advantage in memory comparison because they are typically associated with fewer alternative long-term memory codes. It is also important to note the size of the intercept values for the letter probes (?z = 720 msec) reported by Klatzky and Atkinson. A representative sample of memory-search studies that also used letter stimuli

*According to the logic of interpretation developed by MOSCOVITCH [lS], one aspect of the present data is not consistent with a relative efficiency model. When both hemispheres contribute to a particular decision, any VF difference that is present should interact statistically with response hand. since any processing advantage of a given hemisphere will be magnified when this hemisphere also controls the hand of response. In the present experiment, however, the right VF advantage for the slope values was independent of response hand. One possible reason for this discrepancy is that, in Moscovitch’s model. the VF by response hand interaction is determined by the interhemispheric transfer that is necessary when the processing required by the task and the manual response are controlled by different hemispheres. This transfer is associated with the response stage of a RT task. Since factors which are associated only with the response stage of the memory-search pardigm would not be expected to affect the comparison stage [22], a VF by hand interaction may not necessarily appear in the RT data, even though both hemispheres are in fact involved in the comparison process. Thus, the VF by memory-set size interaction and the VF by response hand interaction are separate tests of the functional localization model.

HEMISPHERIC DIFFERENCES IN MEMORY

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[28-301 has a mean intercept of 455 msec; the mean intercept in the present data is 489 msec. Slope values with alphanumeric stimuli are typically only 3&40 msec in magnitude, and reliable VF differences in slope may be difficult to observe when the intercept has been drastically raised, as in [16] and [17]. Although the results of the present task indicate that both hemispheres are involved in memory search, alternative interpretations can be developed that are consistent with a functional localization model. For example, it is possible that the comparison stage is carried out solely by the left hemisphere, but that the probe representation developed by the right hemisphere differs more (along some categorical dimension) from the items held in memory than does the probe processed by the left hemisphere. This situation could lead to an increased slope for the left VF probes, since CRUSE and CLIFTON [3 l] have observed that, in a memory-search task, the slope increases when the probe and memory-set items are presented in different “formats” (e.g. octal vs binary numbers). At the present time such alternative explanations lack parsimony, because they require detailed assumptions about the nature of the hemispheric coding processes involved in the memory-search task. However, such assumptions certainly merit empirical investigation, since it is unlikely that either a functional-localization or a relative-efficiency model alone will be sufficient to characterize performance on all cognitive tasks. Future research should be directed at defining the nature of the task requirements for which each model is appropriate. ,1c~nowledgements~This research was supported by NIA Postdoctoral Fellowship No. 5 F32 AGO51 19-2, NIA Training Grant No. AGO0029, and NINDS Grant No. 06233. The authors thank JOSEPH B. HELLIOE and MORRIS MOSCOVITCH for their comments on an earlier version of the manuscript.

REFERENCES 1. M~SCOVITCH, M. Information processing and the cerebral hemispheres. In Handbook of Behavioral Neurobiology, I/or. 2: Neuropsychology, M. S. GAZZANIC;A (Editor). Plenum Press, New York, 1979. 2. MADDEN, D. J. and NEBES, R. D. Visual perception and memory. In The Brain and Psychology, M. C. WITTROCK (Editor). Academic Press, New York, 1980. 3. KIMURA, D. and D~RNFORD, M. Normal studies on the function of the right hemisphere in vision. In Hemisphere Function in the Human Brain, S. J. DIMOND and J. G. BEAUMONT (Editors). John Wiley, New York, 1974. 4. HINES, D., SATZ, P., STHELL, B. and SCHMIDLIN,S. Differential recall of digits in the left and right visual half-fields under free and fixed order of recall. Neuropsychologia 7, 13-22, 1969. 5. HINES, D. and SATZ, P. Superiority of right visual half-fields in right-handers for recall of digits presented at varying rates. Neuropsychologia 9, 21-25, 1971. Hrr~s, D., SATZ, P. and CLEMENTINO,T. Perceptual and memory components of the superior recall of letters from the right visual half-fields. Neuropsychologia 11, 175-180, 1973. HANNAY, H. J. and MALONE, D. R. Visual field effects and short-term memory for verbal material. Neuropsycholoyia 14, 203-209, 1976. M~SCOVITCH, M., SCULLION, D. and CHRISTIE, D. Early versus late stages of processing and their relation to functional hemispheric asymmetries in face recognition. J. cup. Psycho!.: Hum. Percept. Performancr, 2, 401.-416, 1976. 9. STERNBERG,S. High-speed scanning in human memory. Science 153, 652-654, 1966. 10. STERNRERC;,S. Memory scanning: New findings and current controversies. Q. J. exp. Psycho/. 27, l-32, 1975. 11. BRIGCIS,G. E. and SWANSON,J. M. Encoding, decoding, and central functions in human information processmg. J. exp. Psycho/. 86, 296-308, 1970. 12. TOWNSEW, J. T. A note on the identifiability ofparallel and serial processes. Percept. Psychophys. IO, 161- 163, 1971. 13. THEIOS, J. Reaction time measurements in the study of memory processes: Theory and data. In The Psychology qflraming and Mofiuation, Vol. 7, G. H. BOWER (Editor). Academic Press, New York, 1973. 14. MOSCOVITCH, M. On the representation of language in the right hemisphere of right-handed people. Brain & Language 3,47-71, 1976. 15. MOSVOVIT(.H, M. Language and the cerebral hemispheres: Reaction time studies and their implications for models of cerebral dominance. In Communication and @xr: Language and Thought, P. PLINER, T. ALL~WAY and L. KRAMES (Editors). Academic Press, New York, 1973.

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16. KLATZKY, R. L. Interhemispheric transfer of test stimulus representations in memory scanning. Psq’chon. Sci. 21, 201-203, 1970. 17. Ki ATZKY, R. L. and ATKIUSON, R. C. Specialization of the cerebral hemsipheres in scanning for information in short-term memory. Percept. Psychophys. 10, 335- 33X. 1971. 1X. SK~ALOWI~Z. S. J. and STF..MAR I. c‘. Left and right lateralization for letter matching: strategy and sex differences. NeuropsJcholoyiu 17, 521-525. 1979. 19. STf.RNwRci, S. Two operations in character recognition: Some evidence from reaction-time measurements. Prrccpt. Psychophys. 2, 45 53. 1967. effects on reaction time to verbal and 20. GPFEN, G., BRAIXHA\\~, J. L. and WALLAU 1 G. Interhemispheric nonverbal visual stimuli. J. c.xp, P.syc,ho/. 87, 415 422. 1971. 21. HFLLKF, J. B. Effects ofperceptual quality and visual field of probe stimulus presentation on memory search for letters. J. op. Psycho/.: Hum. Prrwpt. Pr~t$vt~~trncc~.in press. 22. STtRNRtRG, S. The discovery of processmg stages: Extensions of Donders’ method. In .Attcutim cd Pr~formunc~ II, W. G. Kosr I K (Editor). .Ac,ttr P.s_yho/. 30, 276 315, 1969. 23. DAY, J. Right-hemisphere language processing m normal right-handers. J. rxp. Psycho/.: Hum Percept. Prrformuwe

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differences in a letter classification task. Pc,rcc,pt. P.sychoph,~s. in same different laterality patterns as a function of practice

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M. C’hoice reaction-time study assessing the verbal behavior of the minor hemisphere in normal 27. Mowovfrc~H. humans. J. camp. phpsiol. Psycho/. 80, 66 74. 1972. 2X. C%Asr:, W. CT.and Chi.Ff-E. R. C. Modality and sjmilarlty effects in short-term recognition. J. c)up. Psycho/. 81, 510 514, 1969. recognition with digits and letters. Ps~hon. Sri. 20, 29. Yw, J. H. and SANTA, J. L. Reaction time in short-term 121-122, 1970. B. L. and PA~HFI IA, R. G. The effect of memory load on reaction time in character 30. WATTENBARGFR. classification. Perwpr. P,sychoph~~ 12, 100 102, 1972. from memory. Coq. Psycho/. 4, 31. CRLw, D. and Ci IFTOY, C. Recoding strategies and the retrieval of information 157 193, 1973.

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IN MEMORY

Zusammenfassung Jiingere einen

Befunde

Beitrag

Liefern.

Das

legen

die Annahme

gegenwartige

Experiment

die verbale

Gedgchtnis

stellten.

Die Ergebnisse

im rechten

Gesichtsfeld/links

nicht

assoziiert

mit dem war.

Leistungsfahigkeit der

da13 Anforderungen

zu den Gesichtsfeldunterschieden

Versuchsanordnung,

aber

nahe,

funktionellen

der

Ergebnisse

(Zahlen)

zeigten

Hemisphgre,

wahrnehmungsmafligen

Diese

bei tachistoskopischem

untersuchte

Stimuli

lassen

einen

besser

Vorteil

erklaren

an das

bei Darbietung

im Ged?ichtnis,

und Antworten durch

in einer

und Anforderungen

signifikanten

Enkodieren sich

Erkennen

Gesichtsfeldunterschiede benutzte

der mit dem Vergleich

Hemispharenspezialisierung

Lokalisation.

an die Merkfahigkeit

ein Model1

der Aufgabe der relativen

als mit einem

Model1