source memory impairment in patients with frontal lobe lesions

Neuropsycholoyia, Vol. 27, No. 8, pp. 1043 1056, 1989, 0028 3932/89 $3,00+0.00 Printed in Great Britain. Pergamon Press plc

S O U R C E M E M O R Y I M P A I R M E N T I N P A T I E N T S W I T H

F R O N T A L L O B E L E S I O N S

JERI S. JANOWSKY,* A R T H U R P . SHIMAMURA a n d LARRY R. SQUIRE~"

Veterans Administration Medical Center and Depar tment of Psychiatry, University of California, San Diego, La Jolla, CA 92161, U.S.A.

(Received 30 June 1988; accepted 1 December 1988)

Abst rac t - - In two experiments, we investigated memory for recently learned facts and memory for the source of the facts (i.e. where and when the facts were learned) in patients with frontal lobe lesions, age-matched elderly control subjects, and younger subjects. In both experiments, patients with frontal lobe lesions recalled as many facts as their age-matched subjects and the younger subjects, but they frequently attributed facts to incorrect sources. In the second experiment, both patients with frontal lobe lesions and their age-matched subjects committed more source errors than younger subjects. These findings suggest that the frontal lobes may play a special role in associating facts to the context in which they were learned. The results are also discussed in the light of the source memory impairment that occurs in amnesic patients.

I N T R O D U C T I O N

IN EVERYOAY situations, one often remembers a fact (e.g. a news item, a research finding) but forgets the source of the information (i.e. where or when the fact was encountered). This distinction between memory for facts and memory for contextual information has been usefully applied to findings with normal subjects. For example, TULWNG [-34, 35] distinguishes between semantic (generic) memory and episodic (autobiographical) memory. Neuropsychological studies show that some amnesic patients exhibit a larger deficit in source or contextual memory than would be expected from their fact memory ability. Thus, they recall a small amount of factual information that was acquired in a recent learning session but then cannot recall where or when the information was learned [24, 28]. This phenomenon has been termed source amnesia [3, 24]. The severity of source amnesia is not inextricably linked to the severity of the fact memory impairment, because patients who showed considerable source amnesia had about the same level of fact memory ability as patients who showed less source amnesia [28].

Source amnesia may be a special case of impaired memory for temporal context. In addition to source amnesia, some amnesic patients (particularly patients with Korsakoff's syndrome) exhibit disproportionate impairment of memory for temporal context relative to their impaired memory for test items (for review, see [13]). For example, patients with Korsakoff's syndrome have particular difficulty identifying which of two sentences was presented more recently [6, 8, 9, 15, 30]. Impaired performance on tests of recency is unlikely

*Current address: Psychology Department , University of Oregon, Eugene, OR 97403-1227, U.S.A. fTo whom correspondence should be addressed: Depar tment of Psychiatry (V116-A), Veterans Administration

Medical Center, 3350 La Jolla Village Drive, San Diego, CA 92161, U.S.A.

1043

1044 JERI S. JANOWSKY, ARTHUR P. SHIMAMURA and LARRY R. SQUIRE

to resul t s imply f r o m w e a k m e m o r y . Specif ical ly , pa t i en t s wi th K o r s a k o f f ' s s y n d r o m e

exh ib i t ed p o o r e r recency j u d g e m e n t s t h a n c o n t r o l subjects , even w h e n i t em r e c o g n i t i o n

m e m o r y was e q u a t e d for the t w o g r o u p s by tes t ing the c o n t r o l subjects af ter a l o n g r e t e n t i o n

in te rva l [15] . M o r e o v e r , o t h e r amnes i c pa t i en t s w h o exh ib i t ed as m u c h i m p a i r m e n t o n tests

of i t em r e c o g n i t i o n m e m o r y as pa t i en t s wi th K o r s a k o f f ' s s y n d r o m e did n o t exh ib i t a

d i s p r o p o r t i o n a t e defici t in t e m p o r a l c o n t e x t m e m o r y [30, 32]. F ina l ly , whi le pa t i en t s wi th

K o r s a k o f f ' s s y n d r o m e were p o o r at iden t i fy ing f a m o u s voices , they were pa r t i cu l a r ly

i m p a i r e d at iden t i fy ing the t ime pe r iod in wh ich the vo ice was k n o w n [16] .

S o m e of these defici ts in t e m p o r a l c o n t e x t m e m o r y are also o b s e r v e d in pa t i en t s wi th

f ron ta l lobe les ions (for reviews, see [18, 25, 31]). F o r e x a m p l e , pa t i en t s wi th f ron ta l lobe

les ions h a d diff icul ty m a k i n g recency j u d g e m e n t s (Cors i , c i ted in MILNER [17]) , e v e n t h o u g h

thei r r e c o g n i t i o n m e m o r y for i tems was no t i m p a i r e d . T h e y also had diff icul ty d e t e r m i n i n g

h o w m a n y t imes s t imul i were p re sen t ed (i.e. diff icul ty wi th f r equency j u d g e m e n t s ) [29] .

F ina l ly , pa t i en t s wi th f ron ta l l obe les ions h a d diff icul ty o r g a n i z i n g a s equence of se l f -o rdered

responses [19] . These defici ts in o r d e r i n g o r s e q u e n c i n g t e m p o r a l i n f o r m a t i o n o c c u r desp i te

the fact tha t pa t i en t s wi th f ron ta l l obe les ions are n o t g loba l ly amnes ic . I ndeed , o n s t a n d a r d

tests of recal l a n d r e c o g n i t i o n m e m o r y , they p e r f o r m m u c h be t t e r t h a n amnes i c pa t i en t s a n d

of ten as well as a g e - m a t c h e d c o n t r o l subjects [11] .

If sou rce m e m o r y is r e l a t ed to m e m o r y for t e m p o r a l con tex t , then pa t i en t s wi th f ron ta l

lobe les ions m i g h t be expec ted to h a v e i m p a i r e d source m e m o r y . W e e x a m i n e d fact m e m o r y

and source m e m o r y in pa t i en t s wi th f ron ta l l obe les ions , a g e - m a t c h e d e lder ly c o n t r o l

subjects , a n d y o u n g e r subjects . In E x p e r i m e n t 1, fact and source m e m o r y were assessed af ter

a 6 -8 day delay . In E x p e r i m e n t 2, we p re sen t ed facts inc iden ta l ly a n d tes ted m e m o r y af ter a

5 min and 2 h r delay.

E X P E R I M E N T 1 - - M E T H O D

Subjects

Patients with frontal lobe lesions. Seven patients with lesions of the frontal lobes were identified by review of medical records and CT scans at the VA Medical Center, San Diego, and at the University of California, San Diego Medical Center. Five patients with unilateral frontal lobe lesions (2 left, 3 right) and two patients with bilateral lesions were studied (Fig. 1). All had lesions restricted to the frontal lobes, and none had other diagnoses likely to affect cognition or interfere with participation in the study (e.g. significant psychiatric disease, alcoholism). A detailed description of these patients appears elsewhere [11].

These seven patients (four men and three women) averaged 63.9 yr of age (range = 44-71 ), had 13.0 yr of formal education (range = 8 18), and an average Wechsler Adult Intelligence Scale-Revised (WAIS-R) Full Scale IQ score of 101.1 (range = 85 118). A detailed report of the neuropsychological findings for these patients appears elsewhere [ ! 1 ]. Briefly, they were impaired on the Wisconsin card sort test [2, 7], a standard test of frontal lobe dysfunction. In addition they were impaired on the Initiation Perseveration index of the Dementia Rating Scale [-12], and the patients with left or bilateral frontal lobe lesions had impaired verbal fluency (Table 1 summarizes these results for each patient). The patients also exhibited normal performance on other standard neuropsychological tests including tests of language, memory, and perception. Testing occurred between February and August, 1987.

Older subjects. Nine older subjects (4 women and 5 men) were also studied. One subject was the spouse of a study patient. The others were volunteers or employees at the VA Medical Center. They were matched to the patients with frontal lobe lesions with respect to age (mean = 63.9, range = 55 79) and education (mean = 12.8, range = 12 16). They were also matched with respect to two WAIS-R subtest scores, Information (mean = 20.9; mean = 21.9 for the patients with frontal lobe lesions) and Vocabulary (mean = 53.0; mean = 53.7 for the patients with frontal lobe lesions). Their average WAIS-R Full Scale IQ score was 105.1.

Younyer subjects. Seven younger subjects (5 women and 2 men, mean age-49.4 yr, range 42-57) served as a comparison group. They were also volunteers or employees at the VA Medical Center. They were matched to the patients with frontal lobe lesions with respect to education (mean = 14.3 yr, range = 12 16) and also with respect to two WAIS-R subtest scores, Information (mean = 22.3) and Vocabulary (mean = 52.4).

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SOURCE MEMORY IMPAIRMENT IN PATIENTS WITH FRONTAL LOBE LESIONS

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Fie. 1. Reconstructions of the frontal lobe damage (in black) from the CT or MRI brain scans of each patient in the study, using the method of H. Damasio (1983, and personal communication). The most ventral section is shown at the top of each series of sections. The lateral view below each reconstruction shows the angle of the horizontal sections and the locations of the most dorsal and

ventral sections.

Materials

The materials and procedure for this study were the same as those used in a previous study of source memory in amnesic patients ([28], Experiment 1). Briefly, 30 difficult general-information questions were compiled from reference books and the NELSON and NARENS [21] norms and printed on index cards. These were divided into 3 sets of 10 questions each. Two sets of the questions were presented during both the study and retention test, and the third set was presented only during the retention test in order to assess how much knowledge subjects had about the material prior to testing. The three sets were rotated across the study and test conditions so that every three subjects formed a completely counterbalanced group.

1046 JERI S. JANOWSKY, ARTHUR P. SH1MAMURA and LARRY R. SQU1RE

TABLE 1. Neuropsychological test profile of patients with frontal lobe lesions

Patient

Wisconsin Verbal card sort MQ Init/pers fluency

No. categories WMS DRS (percentile) Lesion

J,D. 5 135 78 65 R.L. 3 112 70 5 J,V. 4 102 97 80 M.S. 0 86 97 50 E.M. 2 118 97 90 G.Y. 1 96 76 4 M.D. 0 97 86 10

Mean 2.1 107.4 85.9 43

Left dorsolateral prefrontal Left dorsolateral prefrontal Right dorsolateral prefrontal Right dorsolateral and oribtal prefrontal Right medial prefrontal Bilateral frontal Bilateral frontal

MQ WMS--Memory Quotient, Wechsler Memory Scale. Init/Pers DRS--Init iat ion and Perseveration index of Dementia Rating Scale.

Procedure

Subjects were told that they would be asked to learn some general-information facts. In order to select facts that were not known prior to the study session, each fact was first presented on a card in the form of a question (e.g. What was the last name of the actor who portrayed Dr Watson in the Sherlock Holmes series?). If the subject answered a question correctly, that question was discarded and another was substituted in its place. Ten questions of comparable difficulty to the 20 test questions were available as substitutes when a subject knew the answer to any of the test questions. If the subject was unable to answer the question, the answer was provided by the experimenter in the form of a factual statement (e.g. The last name of the actor who portrayed Dr Watson in the Sherlock Holmes series was Bruce), and the subject was asked to repeat the answer and remember it. Questioning continued until the subject had been given the answers to 20 previously nonrecalled questions. These factual statements were then presented and read to each subject a second time.

After a 6-8 day retention interval, fact recall, source recall and fact recognition memory were tested. During the test phase, no reference was made to the previous study phase. Rather, subjects were simply asked to answer some general-information questions. They were asked a total of 40 questions: the 20 questions (previously nonrecalled) from the study phase, as well as 10 new questions from the same level of difficulty and 10 easy questions that had not been presented previously. The easy questions were presented so that some correctly answered questions would have been learned from a source outside the experimental situation. The 20 previously presented facts and the 20 new facts were presented in random order.

When subjects correctly answered a question, they were asked to recollect where the information had been learned ("That's correct. Can you tell me where you learned the answer?"). In addition, subjects were asked "When was the most recent time you heard that information?". Thus, even ifa subject thought that a fact presented during the study phase had been encountered prior to the study phase, the subject was asked to identify the learning session as the most recent source for that information. Two types of source errors were recorded. An "extraexperimental source error" could occur for any of the 20 questions presented during the study phase that were answered correctly during the test phase. An "extraexperimental source error" was recorded if the subject reported that the information was most recently learned from an outside source, when it had in fact been presented during the study phase. An "experimental source error" was recorded if the subject reported that the information had been learned in the study phase when in fact it had not been presented previously [24]. An "experimental source error" could occur for any of the 20 new questions that were answered correctly (10 baseline questions and 10 easy questions). Following the tests of recall and source memory, an 8-alternative forced-choice recognition test was administered for all 40 items.

E X P E R I M E N T 1 - - R E S U L T S

F i g u r e 2 s h o w s f ac t r e ca l l a n d r e c o g n i t i o n p e r f o r m a n c e f o r t h e p a t i e n t s w i t h f r o n t a l l o b e

l e s i o n s , t h e o l d e r s u b j e c t s , a n d t h e y o u n g e r s u b j e c t s . B o t h r eca l l a n d r e c o g n i t i o n w e r e s i m i l a r

a c r o s s g r o u p s ( F s < l . 6 1 , P s > 0 . 1 0 ) . D u r i n g t h e s t u d y s e s s i o n , s u b j e c t s in e a c h g r o u p

a n s w e r e d c o r r e c t l y a s i m i l a r n u m b e r o f q u e s t i o n s in t h e c o u r s e o f i d e n t i f y i n g 20 n o n r e c a l l e d

q u e s t i o n s ( m e a n s - - 2 3 . 4 , 22 .8 a n d 25 .0 q u e s t i o n s fo r t h e p a t i e n t s w i t h f r o n t a l l o b e l e s i o n s ,

o l d e r s u b j e c t s a n d y o u n g e r s u b j e c t s , r e s p e c t i v e l y ) . P e r f o r m a n c e w a s a l s o s i m i l a r a c r o s s

g r o u p s f o r r e ca l l a n d r e c o g n i t i o n o f t h e 20 n e w q u e s t i o n s t h a t h a d n o t b e e n p r e s e n t e d fo r

SOURCE MEMORY IMPAIRMENT IN PATIENTS WITH FRONTAL LOBE LESIONS 1047

I00

9O

8O

70

60

50

40

50

2O

I0

0

RECALL OF F A C T S RECOGNITION OF FACTS

I T

T T

T

F 0 F 0 Y

FIG. 2. Fact recall (left) and recognition (right) by patients with frontal lobe lesions (F), older subjects (O), and younger subjects (Y) tested after a 6-8 day retention interval. Brackets show SEM.

study (Fs< l .60 , Ps>0.10) . Thus, patients with frontal lobe lesions had comparable background knowledge to older and younger subjects and were as capable as these subjects at learning and remembering new material.

Figure 3 shows the overall percentage of source errors committed by the three groups. For this score, extraexperimental and experimental source errors were combined. The overall percentage of source errors therefore reflects the number of source errors committed for all the questions from the set of 40 that were answered correctly (20 studied items, 10 new items and 10 easy items). The performance of the three groups differed significantly (F 1-2, 20] = 7.31, P < 0.01). Post-hoc analyses revealed that the patients with frontal lobe lesions committed significantly more source errors than either the older subjects (t [ 14 ]=2 .45 , P < 0 . 0 5 ) or the younger subjects (t [ 12 ]=3 .27 , P<0 .01) . The older and younger subject groups did not differ from each other (t [14] = 1.57, P>0 .10) .

4 0

~) 30

w

~ 20

~ io

OVERALL EXTRAEXPERIMENTAL EXPERIMENTAL SOURCE ERRORS SOURCE ERRORS SOURCE ERRORS

T

F Y 0 Y F 0 Y

FIG. 3. Source memory performance by patients with frontal lobe lesions (F), older subjects (O) and younger subjects (Y) tested after a 6-8 day retention interval. The percent of overall source errors (left) reflects both extraexperimental and experimental source errors (right). Brackets show SEM.

1048 JER1 S. JANOWSKY, ARTHUR P. SH1MAMURA and LARRY R. SQUIRE

E x t r a e x p e r i m e n t a l and e x p e r i m e n t a l source e r ro rs were c o m p a r e d sepa ra t e ly ac ross

g roups , T h e p e r c e n t a g e of e x t r a e x p e r i m e n t a l sou rce e r ro r s reflects the n u m b e r o f source

e r ro rs c o m m i t t e d whi le a n s w e r i n g the 20 q u e s t i o n s tha t had been p re sen t ed in the s tudy

phase ( n u m b e r of source e r r o r s / n u m b e r of q u e s t i o n s a n s w e r e d cor rec t ly ) . F o r ex t r aexpe r i -

m e n t a l source e r rors , the dif ference b e t w e e n g r o u p s was n o t s igni f icant (F [2, 20] = 1.45,

P > 0.10), a n d n o n e of the pa i rwise c o m p a r i s o n s r eached s igni f icance (ts < 1.38, Ps > 0.10).

T h e p e r c e n t a g e of e x p e r i m e n t a l source e r ro rs reflects the n u m b e r of source e r ro r s c o m m i t t e d

whi le a n s w e r i n g the 10 new q u e s t i o n s a n d the 10 easy ques t i ons tha t had n o t been p re sen t ed

in the s tudy phase ( n u m b e r of source e r r o r s / n u m b e r o f q u e s t i o n s a n s w e r e d cor rec t ly ) . F o r

e x p e r i m e n t a l sou rce e r ro rs , the g r o u p s differed (F [2, 20] = 4.77, P < 0.05). T h e pa t i en t s wi th

f ron ta l l obe les ions c o m m i t t e d m o r e e x p e r i m e n t a l source e r ro rs t h a n e i the r of the o t h e r two

g r o u p s (ts > 2.20, Ps <0 .05 ) .

Because s o m e subjects rare ly m a d e source e r ro rs , n u m e r o u s ze ros a p p e a r e d in the da ta ,

and the d i s t r i bu t i ons were n o t n o r m a l . H o w e v e r , wi th one excep t ion , the resul ts were s imi la r

us ing n o n p a r a m e t r i c tests. T h e pa t i en t s wi th f ron ta l l obe les ions still m a d e s ign i f ican t ly m o r e

source e r ro r s t h a n the o lde r and y o u n g e r g r o u p s ( K r u s k a l - W a l l i s , H ( 2 ) = 9 . 7 1 , P < 0 . 0 1 ;

M a n n - W h i t n e y U, Us < 12, P < 0.05), bu t n o w the g r o u p s d id n o t differ s ta t i s t ica l ly in t e rms

of the n u m b e r of e x p e r i m e n t a l source e r ro rs c o m m i t t e d ( K r u s k a l - W a l l i s H ( 2 ) = 4 . 5 1 ,

P = 0 . 1 1 ) .

E x p e r i m e n t 1 d e m o n s t r a t e d source m e m o r y i m p a i r m e n t in pa t i en t s wi th f ron ta l l obe

les ions w h e n m e m o r y was assessed after a 6 - 8 day r e t e n t i o n in te rva l . N o r m a l subjects ra re ly

c o m m i t t e d these e r rors . These f indings sugges t tha t the f ron ta l lobes m a y p lay a specia l role

in m e m o r y for sou rce i n f o r m a t i o n . A p r e v i o u s s tudy of amnes i c pa t i en t s s h o w e d tha t sou rce

e r ro rs o c c u r r e d f r equen t ly w h e n i n f o r m a t i o n was p re sen t ed inc iden ta l ly , even at sho r t

r e t e n t i o n in te rva l s [28] . In the s econd e x p e r i m e n t , we p resen ted facts inc iden ta l ly and tes ted

fact m e m o r y a n d source m e m o r y af ter b o t h 5 rain and 2 hr de lay in te rva ls .

E X P E R I M E N T 2 - - M E T H O D S Subjects

Patients with frontal lobe lesions. See Experiment 1. Older subjects. Eight of the nine subjects from Experiment 1 participated in this study together with one new

subject. They averaged 62.2 yr of age (range = 55 68) and 13.2 yr of education (range = 12 16). They matched the study patients with respect to two WAIS-R subtest scores (Information: mean = 21.2, Vocabulary: mean = 53.3).

Youn,qer subjects. Five new subjects and one subject who had also participated in Experiment 1 (5 women and 1 man, mean age = 51.0 yr) served as an additional comparison group. They were volunteers or employees at the VA Medical Center. They matched the patients with respect to education (mean = 14.3 yr). They also matched the study patients on the basis of two WAIS-R subtest scores (Information: mean- 20.5, Vocabulary: mean = 55.3).

Materials

The materials and procedure for this study were the same as those used in a previous study of source memory in amnesic patients ([28], Experiment 2). Briefly, 30 obscure facts (e.g. the body of water that lies between Russia and Iran is the Caspian Sea) were compiled from books on trivia and from encyclopedias. The facts were divided into two sets of fifteen each. Each set contained three facts from each of five categories: books and comics, movies and plays, history, geography, and sports. One set was presented in the study phase. The other was used in the test phase to assess baseline level of recall. The two sets were counterbalanced across the study and baseline test conditions. Four easy factual questions were also included in the test phase (e.g. What is the name of a dried grape? [raisin]). The easy questions were included so that some of the correctly answered questions would have been learned from a source outside the experimental situation.

Procedure

During presentation of the facts in the study phase, subjects were told that this was a study of how people categorize information. No instructions were given to learn and remember the material. Subjects were asked to read

S O U R C E M E M O R Y I M P A I R M E N T I N P A T I E N T S W I T H F R O N T A L LOBE LESIONS 1049

each fact aloud from a printed card and to place each card in one of five categories. Cards showing each category name were arranged on a table in front of the subject. The task was self-paced. After the 15 facts were sorted, the fact cards were shuffled and the category names were rearranged on the table. The subject was then asked to read the facts and to categorize them once again.

After a 5 min retention interval, fact recall, source recall and recognition memory were tested. The facts were now presented in the form of questions (e.g. What body of water lies between Russia and Iran?). The retention test included the 15 facts that had been presented previously, 15 new (baseline) facts that had not been presented, and 6 new easy facts for a total of 36 questions. The procedures for recall, source recall, and recognition were identical to Experiment 1. As in Experiment 1 no reference was made to the study phase during the test phase. Only eight of the nine older subjects and five of the six younger subjects participated in this part of the experiment.

On another occasion the patients with frontal lobe lesions, the older subjects, and the younger subjects were also tested using a second similar set of materials. The procedure for this test was identical to the test just described, except that retention was tested after 2 hr instead of after 5 rain. Also, whereas in the previous test six "easy" questions were asked, in this case only four "easy" questions were asked for a total of 34 questions. Across subjects, the 5 min delay condition and 2 hr delay condition were separated by an average of 52 days (minimum = 12 days).

E X P E R I M E N T 2 - - R E S U L T S

Five minute delay condition

F i g u r e 4 s h o w s fac t reca l l a n d r e c o g n i t i o n p e r f o r m a n c e in the 5 m i n d e l a y c o n d i t i o n fo r t he

p a t i e n t s w i t h f r o n t a l l o b e l e s ions , t he o l d e r s u b j e c t g r o u p , a n d t he y o u n g e r s u b j e c t g r o u p .

B e c a u s e l e a r n i n g w as i n c i d e n t a l , we c o u l d n o t p r e s c r e e n the fac ts to d e t e r m i n e if s u b j e c t s

c o u l d reca l l t h e m p r i o r to t he s t u d y p h a s e . F o r s t a t i s t i c a l p u r p o s e s , fac t l e a r n i n g ( recal l a n d

r e c o g n i t i o n ) w as c a l c u l a t e d as t he p e r c e n t c o r r e c t sco re for t he 15 p r e v i o u s l y p r e s e n t e d facts

m i n u s t he p e r c e n t c o r r e c t sco re for t he 15 n e w ( b a s e l i n e ) facts . P a t i e n t s w i t h f r o n t a l l o b e

l e s ions p e r f o r m e d s i m i l a r l y to t he o l d e r a n d y o u n g e r s u b j e c t s ( for recal l , F [2, 17] = 2.57,

P > 0 . 1 0 ; for r e c o g n i t i o n , F [ 2 , 17] = 2 . 1 9 , P > 0 . 1 0 ) . T h u s , as in E x p e r i m e n t 1, t he p a t i e n t s

w i t h f r o n t a l l o b e l e s ions were as c a p a b l e o f l e a r n i n g a n d r e m e m b e r i n g n e w m a t e r i a l as t he

o t h e r t w o s u b j e c t g r o u p s .

I00 RECALL OF FACTS

90

8O

f'O , I

~o ~ 5O

4 0 ,

~©

~

, o

© ~,~*: :: :

F 0 5'

RECOGNITION OF FACTS

l, -[--

F 0 Y

FIG. 4. Fact recall (left) and recognition (right) by patients with frontal lobe lesions (F), older subjects (O), and younger subjects (Y) tested 5 min after an incidental learning task. The stippled areas show

baseline recall and recognition performance. Brackets show SEM.


Figure 5 shows the overall percentage of source errors committed by each group in the 5 min delay condition. The overall percentage of source errors reflects the total number of source errors committed for those questions answered correctly out of all 36 questions asked during the retention test (15 studied items, 15 new items, and 6 easy items). The performance of the groups differed significantly (means= 10.9%, 9.4% and 3.0% for the patients with frontal lobe lesions, the older subjects, and the younger subjects, respectively; F I-2, 17] =5.21, P<0.05) . Post-hoc analyses revealed that the patients with frontal lobe lesions and the older subject group committed significantly more source errors than the younger subject group (ts > 2.45, Ps < 0.05), but patients with frontal lobe lesions did not differ significantly from the older subject group (t [13] = 0.65, P > 0.10). Each type of source error was also compared across groups. For extraexperimental and experimental source errors, the difference between groups was not significant (Fs [2, 17] < 0.95, Ps > 0.10).

¢~ 30

o~ ~0

i~

~ ~o

40 EXTRAEXPERIMENTAL EXPERIMENTAL SOURCE ERRORS SOURCE ERRORS

OVERALL SOURCE ERRORS

T

F 0 Y

i

F 0 F 0 ¥

FIG. 5. Source memory performance by patients with frontal lobe lesions (F), older subjects (O), and younger subjects (Y) 5 min after an incidental learning task. The percent of overall source errors (left)

reflects both extraexperimental and experimental source errors (right). Brackets show SEM.

As in Experiment 1, the distributions were not normal because some subjects rarely made source errors and numerous zeros appeared in the data. However, the results remained the same using nonparametric tests.

Two hour delay condition

Figure 6 shows fact recall and recognition performance in the 2 hr delay condition for the patients with frontal lobe lesions, the older subjects, and the younger subjects. As in the 5 min delay condition, fact recall and recognition were calculated for statistical analysis as the percent correct score for the 15 previously presented facts minus the percent correct score for the 15 newly presented facts. Patients with frontal lobe lesions performed similarly to the older and younger subject groups (for recall, F [ 2 , 19]= 1.13, P>0 .10 ; for recognition, F [2, 19] = 1.40, P>0.10) .

Figure 7 shows the overall percentage of source errors committed by each group in the 2 hr delay condition. The overall percentage of source errors reflects the total number of source errors committed for those questions answered correctly out of all 34 questions asked during the retention test (15 studied items, 15 new items, and 4 easy items). The performance of the


bOO

9 0

8 0

7O

b N ~o

5O

N ao ~.

3 0

~ 0

~0

0

RECALL OF F A C T S RECOGNITION OF FACTS

J

F 0 Y

T T

F 0 Y

FIG. 6. Fact recall (left) and recognition (right) by patients with frontal lobe lesions (F), older subjects (O), and younger subjects (Y) tested 2 hr after an incidental learning task. The stippled area shows

baseline recall and recognition performance. Brackets show SEM.

groups differed significantly (means = 24.3 %, 13.8 % and 3.1% source errors for the patients with frontal lobe lesions, the older subjects and the younger subjects respectively; F [ 2 , 19]=5.04 , P<0 .05) . Post-hoe tests revealed that patients with frontal lobe lesions committed significantly more source errors than the younger subject group (t [11] = 3.51, P<0 .01) . The older subject group also committed more source errors than the younger subject group, but this difference fell short of significance (t [ 1 3 ] = 1.84, P=0 .09) . The patients with frontal lobe lesions did not differ from the older subject group (t [14] = 1.52, P>0 .10) .

8

6C

50

4 0

30

20

I 0

0

OVERALL EXTRAEXPERIMENTAL EXPERIMENTAL SOURCE ERRORS SOURCE ERRORS SOURCE ERRORS

T

F O Y

T ~

F O F O Y

FIG. 7. Source memory performance by patients with frontal lobe lesions (F), older subjects (O), and younger subjects (Y) 2 hr after an incidental learning task. The percent of overall source errors (left)

reflects both extraexperimental and experimental source errors (right). Brackets show SEM.


Each type of source error was also compared across groups. The percentage of extraexperimental source errors was marginally significant across groups (F [2, 18] = 3.36, P = 0.06). Post-hoc analyses revealed that the patients with frontal lobe lesions committed significantly more extraexperimental source errors than the younger subjects (t [ 11] = 4.01, P<0.01) . The older subject group also committed more source errors than the younger subject group, but this difference fell just short of significance (t [12] = 1.97, P = 0.07). The patients with frontal lobe lesions and the older subject group did not differ from each other (t [-13] = 0.27, P > 0.10). The percentage of experimental source errors did not differ across groups (F [2, 19]=0.71, P>0.10) .

Again, because numerous zeros appeared in the data, the results were also evaluated using nonparametric tests. The results remained essentially the same with the following exception. The percentage of extraexperimental source errors was significantly different across groups (H [2] = 9.09, P < 0.05; P = 0.06 with parametric tests). Also, both patients with frontal lobe lesions and the older subject group made more extraexperimental source errors than the younger subject group (Us < 8, Ps < 0.05).

D I S C U S S I O N

Experiment 1 showed that source memory was significantly impaired in patients with frontal lobe lesions. Six to 8 days after learning, they were able to recall and recognize factual information as well as normal subjects from two different age groups, but they made significantly more source errors than either of these groups. In Experiment 2, when facts were presented incidentally, patients with frontal lobe lesions exhibited source errors after both a 5 min and a 2 hr retention interval. In this case, the older subjects made as many source errors as the patients with frontal lobe lesions, and these two groups committed significantly more source errors than the younger group. The quality of the source errors was similar in all subjects. For example, subjects stated that they had learned a fact from a newspaper or from TV, when actually it had been learned in the experimental session. Subjects did not err by attributing a fact to some other visit with the experimenter instead of the most recent visit.

The impaired source memory observed in patients with frontal lobe lesions may be an example of impaired memory for temporal context, which has been observed previously following frontal lobe damage (for reviews, see [18, 19, 25]). In particular, patients with frontal lobe lesions seem to have difficulty making recency judgements and in making other kinds of judgements about temporal information. For example, despite good memory for the words in a recently presented list, and despite good memory for past public events, patients with frontal lobe lesions have special difficulty placing list words and past events into the order in which they actually occurred [26]. Impairments in tasks requiring judgements of relative recency and elapsed time have also been reported following frontal lobe damage in nonhuman primates [4, 20] and in rats [10, 22].

Older control subjects exhibited source memory impairment in Experiment 2 but not in Experiment 1. This finding confirms the recent report that source errors can occur in normal elderly subjects [14]. In that study, source memory was impaired together with recall and recognition memory. The findings from Experiment 2 show that source memory can be impaired in the elderly, even when recall and recognition memory are normal.

One reason why older subjects may have deficient source memory is that the frontal lobes and the functions they subserve are especially sensitive to normal aging. Indeed, other cognitive deficits in the aged have been associated with frontal lobe dysfunction. For

SO U RCE MEMORY IMPAIRMENT IN PATIENTS W I T H F R O N T A L LOBE LESIONS 1053

example, both patients with frontal lobe damage and elderly subjects have reduced verbal fluency [23], and they perform more poorly than younger subjects on tasks requiring planning and organization [1]. Moreover, cortical neuronal loss associated with aging occurs prominently in the frontal lobes [5].

The performance of patients with frontal lobe lesions and the elderly control subjects differed between Experiments 1 and 2. These experiments differed in two important ways. In Experiment 1, information was intentionally learned by the subjects and the retention interval was 6-8 days. In Experiment 2, information was presented incidentally and the retention intervals were shorter (5 min and 2 hr). The incidental nature of the learning in Experiment 2 may have increased the difficulty of the task to a level where even the older subjects made source errors.

The types of source errors committed by the patients with frontal lobe lesions varied somewhat between Experiments 1 and 2. In Experiment 1, patients with frontal lobe lesions made extraexperimental source errors but not experimental source errors. That is, the patients misattributed information learned in the study phase to another source, but they did not attribute information to the study phase that had been acquired from another source. By contrast, in Experiment 2 the patients committed both types of source errors, attributing information learned in the study phase to another source as well as attributing information to the study phase that had been learned elsewhere. It may be that the long retention interval used in Experiment 1 made it less likely to attribute information to the study phase. It is also possible that the incidental learning method used in Experiment 2 increased the overall likelihood of committing source errors.

The results are consistent with the idea that the frontal lobes serve to associate information in memory to various aspects of its context. In the present study, it was evident that patients with frontal lobe lesions had both factual knowledge and knowledge about context information. They recalled factual information as readily as normal subjects, and they displayed knowledge about the source of these facts whenever they made a correct source judgement and whenever they committed experimental source errors (i.e. whenever they incorrectly identified the experimental session as the source of information that had not been presented there). This finding suggests that frontal lobe dysfunction causes a disconnection between fact memory and context memory, rather than causing amnesia for the context itself.

Table 2 compares source memory for the patients with frontal lobe lesions and for amnesic patients who were given the same tests in exactly the same manner [28]. The amnesic patients consisted of seven patients with amnesia due to Korsakoff's syndrome, three patients with amnesia due to an anoxic or ischemic episode, and case N. A. They were of normal intelligence (mean I Q = 108.5) and were impaired on the Weschler Memory Scale (mean WMS score = 83.5). Additional neuropsychological test scores for 10 of these 11 patients are reported elsewhere [33]. When the amnesic patients and the patients with frontal lobe lesions were equated for memory strength, the overall percentage of source errors was similar in the two groups (Experiment 1 : amnesic patients tested after a 2 hr delay vs frontal patients tested after a 1 week delay; Experiment 2: amnesic patients tested after a 5 min delay vs frontal patients tested after a 2 hr delay). One important difference between the two groups was that in Experiment 1 patients with frontal lobe lesions made both extraexperimental and experimental source errors, whereas the amnesic patients made only extraexperimental source errors. That is, patients with frontal lobe lesions misattributed study facts to sources outside the experimental session, and they also misattributed nonpresented facts to the experimental session. Amnesic patients misattributed study facts to sources outside the


experimental session, but they rarely stated that a non-presented fact was presented during the session. This qualitative difference between the performance of the two patient groups was reliable, as indicated by a significant group × error type interaction (F [1, 16] = 5.14; P<0.05) . Perhaps amnesic patients do not attribute information learned outside the test session to the test session itself (i.e. they do not commit experimental source errors), because memory is very poor for the test session in which the facts were learned.

TABLE 2. Comparison between patients with frontal lobe lesions and amnesic patients

Fact memory Source memory (Percent correct) (Percent error)

Subject groups Recall recognition Overall Extraexperimental Experimental

Experiment 1 Amnesics (n = 11 ) 31 56 16 45 0

(2 hr delay)

Frontals (n = 7) 41 63 17 15 20 (1 week delay)

Experiment 2 Amnesics (n = 10) 31 54 32 69 7

(5 rain delay)

Frontals (n = 7) 56 75 11 17 4 (5 rain delay)

Frontals ( = 7) 47 71 24 42 2 (2 hr delay)

The data for the amnesic patients is from SHIMAMURA and SQUIRE [28].

The present findings suggest that the source amnesia observed in amnesic patients is due at least in part to frontal lobe dysfunction. Patients with Korsakoff's syndrome, who frequently exhibit source amnesia [28] have frontal lobe atrophy as measured by a quantitative CT scan technique [27], and they resemble patients with frontal lobe lesions on several cognitive tests [11]. In addition, in a mixed group of memory-impaired patients (e.g., head injury, encephalitis, Alzheimer's disease), the degree of source amnesia was correlated with performance on tests sensitive to frontal lobe dysfunction [24]. In that study, four additional patients with frontal lobe damage (two with anterior communicating artery aneurysms and two with left frontal strokes) did not show source errors, and it was concluded that source amnesia requires both severe memory impairment and frontal lobe dysfunction. The group of patients used in the present study demonstrated that source memory impairment can occur in frontal lobe patients in the absence of amnesia.

Certain questions remain about the contribution of frontal lobe dysfunction to source amnesia in amnesic patients. In our previous study, the degree of source memory impairment in amnesic patients was variable and was not restricted to one etiology [28]. For example, source amnesia was observed both in patients with Korsakoff's syndrome, and also in three patients with amnesia due to anoxia or ischemia, even though these latter patients showed little if any neuropsychological evidence of frontal lobe dysfunction [11]. It may be that amnesia itself, in the absence of frontal lobe dysfunction, will produce source amnesia, if memory is so poor that information about the learning context is simply not available. This proposal leads to the prediction that source amnesia should also be observed in normal subjects when context memory is very weak. Previous studies have not found much


ev idence for source m e m o r y i m p a i r m e n t in c o n t r o l subjec ts w h e n c o n t e x t m e m o r y was

w e a k e n e d by tes t ing subjects af ter r e t e n t i o n in t e rva l s as l o n g as 1-2 weeks [24,28] .

Neve r the l e s s , it seems poss ib le t ha t if even l o n g e r r e t e n t i o n in te rva l s were used (e.g. severa l

m o n t h s ) , one m i g h t o b s e r v e sou rce e r ro r s in c o n t r o l subjects , desp i te s o m e p re se rved fact m e m o r y .

In s u m m a r y , pa t i en t s wi th f ron ta l l o b e les ions exh ib i t ed i m p a i r e d sou rce m e m o r y for facts

a c q u i r e d in a recen t test sess ion, even t h o u g h m e m o r y for the facts t hemse lves was n o r m a l .

T h e f indings f r o m o lde r subjec ts s h o w e d tha t sou rce m e m o r y i m p a i r m e n t can a lso o c c u r wi th

n o r m a l ag ing . These f indings s u p p o r t the v iew tha t the f ron ta l lobes are essent ia l for

a s soc i a t i ng i n f o r m a t i o n in m e m o r y to the c o n t e x t in wh ich it was a c q u i r e d . T h e resul ts a lso

s h o w tha t f ron ta l l o b e d a m a g e a lone , in the absence o f i m p a i r e d fact m e m o r y , is suff icient to

i m p a i r sou rce m e m o r y . F ina l ly , these f indings he lp to exp la in the sou rce a m n e s i a tha t is

s o m e t i m e s o b s e r v e d in a m q e s i c pa t i en t s . S o u r c e m e m o r y i m p a i r m e n t m a y o c c u r espec ia l ly in

a s soc i a t i on wi th f ron ta l l o b e p a t h o l o g y . In a d d i t i o n , amnes i c pa t i en t s m a y be expec t ed to

exh ib i t s o m e sou rce e r ro r s even in the absence o f f ron ta l l obe dys func t i on s imply because

they r e m e m b e r the l e a rn ing c o n t e x t so poor ly .

,4 cknowled,qements--The research was supported by the Medical Research Service of the Veterans Administration, NIMH Grant MH24600, the Office of Naval Research, the McKnight Foundation, and an NIMH postdoctoral fellowship MH090290 (J.J.). We thank Joyce Zouzounis, Kim Rivero-Frink and Loni Shutler for research assistance. A preliminary report of these data was presented at the annual meeting of the Society for Neuroscience, 1988.

R E F E R E N C E S

1. ALBERT, M. S. and KAPLAN, E. Organic implications of neuropsychological deficits in the elderly. In New Directionos in Memory and Agino, L. W. POON, J. L. FOZARD, L. S. CERMAK, D. ARENBEERG and L. W. THOMPSON (Editors), pp. 403432. Lawrence Erlbaum, Hillsdale, New Jersey, 1980.

2. BERG. E. A. A simple objective technique for measuring flexibility in thinking. J..qen. Psychol. 39, 15-22, 1948. 3. EVANS, F. J. and THORN, W. A. F. Two types of posthypnotic amnesia: recall amnesia and source amnesia. Int. J.

clin. exp. Hypnosis 14, 162 179, 1966. 4. FUSTER, J. M. The prefrontal cortex: mediator of cross-temporal contingencies. Human Neurobiol. 4, 168 179,

1985. 5. HAUG, H., BARMWATER, U., E6GERS, R., FIS¢~-~R, D., KUHL, S. and SASS, N. L. Anatomical changes in aging

brain: morphometric analysis of the human prosencephalon. In Brain Aoing: Neuropathology and Neuropharmacolooy, J. CERVOS-NAVARRO and H. I. SARKaNDrR (Editors), Vol. 21, pp. 1-12. Raven Press, New York, 1983.

6. HIRST, W. and VOLP~, B. T. Temporal order judgments with amnesia. Brain Cognit. 1, 394-396, 1982. 7. HrATON, R. K. Wisconsin Card Sortin9 Test Manual. Psychology Assessment Resources, Odessa, FL. 8. HUPPERT, F. A. and PIERCY, M. Recognition memory in amnesic patients: effect of temporal context and

familiarity of material. Cortex 12, 3-20, 1976. 9. HUPPERT, F. A. and PIERCY, M. The role of trace strength in recency and frequency judgements by amnesic and

control subjects. Q. J. exp. Psychol. 30, 34(~354, 1978. 10. KESNER, R. P. and HOLBROOK, T. Dissociation of item and order spatial memory in rats following medial

prefrontal cortex lesions. Neuropsychologia 25, 653~564, 1987. 11. JANOWSKY, J. S., SHIMAMURA, A. P., KRITCHEVSKY, M. and SQUIRE, L. R. Cognitive impairment following

frontal lobe damage and its relevance to human amnesia. Bekav. Neurosci., in press. 12. MATa'IS, S. Dementia Rating Scale. In Geriatric Psychiatry I, R. BELLACK and B. KAR,~SU (Editors), pp. 77 121.

Grune & Stratton, New York, 1976. 13. MAYES, A. R., MEUDELL, P. R. and PICKERING, A. Is organic amnesia caused by a selective deficit in

remembering contextual information? Cortex 21, 167 202, 1985. 14. MCINTYRE, J. S. and CRAIK, F. I. M. Age differences in memory for item and source information. Can. J.

Psychol. 42, 175 192, 1987. 15. MEUDELL, P. R., MAYES, A. R., OSTERGAARD, A. and PICKERING, A. Recency and frequency judgements in

alcoholic amnesics and normal people with poor memory. Cortex 21,487 511, 1985.


16. MEUDELL, P. R., NORTHEN, B., SNOWDEN, J. S. and NEARY, D. Long-term memory for famous voices in amnesic and normal subjects. Neuropsychologia 19, 133-139, 1980.

17. MI•NER• B. Interhemispheric di•erences in the l•calizati•n •f psych•l•gical pr•cesses in man. Br. Med. Bull. 27• 272-277, 1971.

18. MILNER, B. and PETRIDES, M. Behavioral effects of frontal lobe lesions in man. Trends Neurosci. 7 (11 ), 403-407, 1984.

19. MILNER, B., PETR1DES, M. and SMITH, M. L. Frontal lobes and the temporal organization of memory. Human Neurobiol. 4, 137 142, 1985.

20. MISHK1N, M. and MANNING, F. J. Non-spatial memory after selective prefrontal lesions in monkeys. Brain Res. 143, 313 323, 1978.

21. NELSON, T. O. and NARENS, L. Norms of 300 general-information questions: accuracy of recall, latency of recall, and feeling-of-knowing ratings. J. Verb. Learn. Verb. Behav. 19, 338 -368, 1980.

22. OLTON, D. S., WENK, G. L., CHURCH, R. M. and MECK, W. H. Attention and the frontal cortex as examined by simultaneous temporal processing. Neuropsychologia 26, 307 318, 1988.

23, SALTHOUSE, T. A. Adult Cognition: An Experimental Psychology of Human Aging. Springer-Verlag, New York, 1982.

24~ SCHACTER, D. L., HARBLUK, J. L. and MCLACHLAN, D. R. Retrieval without recollection: an experimental analysis of source amnesia. J. Verb. Learn. Verb. Behav. 23, 593-611, 1984.

25, SCHACT~R, D. L. Memory, amnesia, and frontal lobe dysfunction. Psychobiology 15 (1), 21 36, 1987. 26. SHIMaMURA, A. P., JANOWSKY, J. S. and SQUIRE, L. R. Memory for temporal order in patients with frontal lobe

lesions and patients with amnesia. Soc. Neurosci. Abstr. 14, 1043, 1988. 27. SHIr~AMURA, A. P., JERNIGAN, T. L. and SQU1R~, L. R. Korsakofl's syndrome: radiological (CT) findings and

neuropsychological correlates. J. Neurosci. 8, 4400-4410, 1988. 28. SHIUAMURA, A. P. and SQt:IRE, L. R. A neuropsychological study of fact memory and source amnesia. J. exp.

Psychol.: Learn. Mere. Cognit. 13, 464-473, 1987. 29. SMITH, M. L. and M1LNER, B. Differential effects of frontal-lobe lesions on cognitive estimation and spatial

memory. Neuropsychologia 22, 697- 705, 1984. 30. SQUIRE, L. R.C•mparis•nsbetweenf•rms•famnesia:s•mede•citsareuniquet•K•rsak•••ssyndr•me.J.exp.

Psychol.: Learn. Mem. Cognit. 8, 56(~571, 1982. 31. SQL'IRE, L. R. Memory and Brain. Oxford University Press, New York, 1987. 32. SQt:IRE, L. R., NADEL, L. and SLATER, P. C. Anterograde amnesia and memory for temporal order.

Neuropsychologia 19, 141 145, 1981. 33. SQt:~RE, L. R. and SHIM,~MURA, A. P. Characterizing amnesic patients for neurobehavioral study. Behav.

Neurosci. 100, 86(~877, 1986. 34. TULV1NG, E. Episodic and semantic memory. In Organization of Memory, E. TULVING and W. DONALDSON

(Editors), pp. 381-403. Academic Press, New York, 1972. 35. "rULVING, E. Elements of Episodic Memory. Clarendon Press, Oxford, 1983.

source memory impairment in patients with frontal lobe lesions

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