Neuropsychologio, Vol. 21. No. 5, PP. 513.524, 1983. Printed m Great Bntain.

0028-3932/8313.00+0.0 1‘ 1983 Pergamon Press Ltd.

EFFECTS OF FRONTAL LOBE LESIONS ON HYPOTHESIS SAMPLING DURING CONCEPT FORMATION*

KEITH D. CICERONET and RONALD M. LAZAR

Psychiatry Service, Department of Neurology, Memorial Sloan-Kettering Cancer Center, New York, U.S.A.; and Department of Psychology, Queens College, CUNY, New York, U.S.A.

and

WILLIAM R. SHAPIRO

Department of Neurology, Memorial Sloan-Kettering Cancer Center, New York, U.S.A

(Accepred 18 March 1983)

Abstract-Thirty-two subjects with unilateral cerebral tumors were assessed for the use of hypotheses and cognitive strategies during a visual discrimination task. Subjects with frontal lobe lesions attained fewer concepts and used fewer appropriate hypotheses than subjects with tumors confined to the posterior hemisphere, although there was no difference in total hypotheses used. Lose-stay errors were committed with greater frequency among patients with frontal lobe lesions, although not all subjects with frontal lobe tumors exhibited this error tendency. The results of hypothesis sampling and a second visual discrimination transfer task suggested that the frontal lobe deficit was related to difficulty in attending to multiple cues and in monitoring feedback to segregate relevant from irrelevant sources of information.

INTRODUCTION

DAMAGE to the frontal lobes frequently leaves basic psychological processes unaffected, while the “higher forms of regulation” of behavior may be severely disturbed [lS]. Early reports of clinical cases described the consequences of human frontal lobe injury as defects in “initiative” [30), “planning capacity” [l, 301, or intellectual “syntheses” [S), although psychometric measures of intelligence were frequently preserved [11, 123.

Subsequent attempts to characterize the frontal lobe conceptual deficit have commonly relied on some variant of a sorting task [ 10,421. Studies of patients with penetrating missile wounds or cerebral neoplasms by TEUBER and his colleagues either failed to find a difference between subjects with pre-Rolandic and post-Rolandic lesions or demonstrated more severe deficits with posterior lesions [2, 32,40,41]. MILNER [22], using a modified version of the Wisconsin Card Sorting Test (WCST), studied patients with cortical resection for the relief of chronic epilepsy and was able to demonstrate clear-cut impairment in patients with dorsolateral frontal lobe lesions relative to all non-frontal control groups. Additional studies of patients with cerebral lesions of diverse etiology have supported the finding that patients with frontal lobe lesions form fewer categories or “concepts” on the WCST and make more

*Portions of this research were presented at the meeting of the Society for Neuroscience, November 5, 1982. tAddress correspondence to: K. D. Cicerone, Department of Neurology, MSKCC, 1275 York Ave, New York,

NY 10021, U.S.A.

513

514 KEITH D. CITERONE, RONALD M. LAZAR and WII.LIAM R. SHAPIRO

perseverative errors than patients with lesions elsewhere in the brain [9,26,37]. MILNER has also suggested that left frontal lobe lesions produce more profound and long-lasting deficits on the WCST than right frontal lobe lesions [22,23], in apparent agreement with the reports of impaired sorting after dominant hemisphere lesions [S, 213. While the dissociation of verbal and spatial deficits after left or right frontal lobe damage, respectively, is fairly well established [3, 13,23, 311, there is less agreement regarding lateralization of the frontal lobe deficit in conceptual ability [9, 22, 26, 371.

The aim of the present investigation was to examine the effects of unilateral frontal lobe tumors on cognitive functioning, using procedures derived from current theories of human concept identification [6,16,17, 351. Within this framework the subject is assumed to select a cue (“hypothesis”) from a (finite) set of stimulus dimensions and then learn to associate a response to that cue with a reinforcement-outcome [35]. An hypothesis represents the mediating process or rule which the subject uses in order to predict subsequent outcomes [16]. Hypothesis testing proceeds such that hypotheses that are confirmed will be maintained; disconfirmation requires resampling from the pool of available hypotheses and evaluating the relevance of an alternative hypothesis. Eventually, this “win-stayjlose-shift” strategy will result in concept identification, as inappropriate hypotheses are systematically eliminated.

In this study we used a modification of LEVINE’S [17] procedure for the identification of subjects’ hypotheses and cognitive strategies during visual discrimination learning, which has previously been useful in describing cognitive impairment in patients with subcortical pathology [27] and temporal lobe resection for chronic epilepsy [36]. Patients with lateralized anterior or posterior cerebral tumors were compared with respect to (a) the use of hypotheses during the course of concept formation; (b) the ability to modify their selection rules and systematically eliminate inappropriate hypotheses; (c) preferences for specific stimulus dimensions and (d) the use of cognitive strategies.

METHOD

Subjects

All patients were recruited from inpatient and outpatient referrals to the Department of Neurology, Memorial Hospital and were seen as part of an ongoing investigation of the psychological consequences of cerebral neoplasms. The majority of patients had been referred for the management of malignant gliomas. The sample reported here consists of patients sequentially accrued to four groups based on the location of a unilateral tumor. Patients with severe aphasia, dementia, metabolic disturbance or medical complications requiring special care were excluded from the study. The presence of “severe aphasia” or “dementia” was based on (a) neurologist’s ratings of language function and mental status from a standard neurologic exam; and/or (b) the patient’s inability to perform standard psychometric tests (e.g. the WAIS). Of the 14 patients excluded under these criteria, 8 had tumors which involved both the anterior and posterior portions of the cerebral hemisphere (i.e. fronto-temporal, fronto-parietal, or fronto-temporo-parietal lesions). Of the remaining 6 patients excluded from study, 3 were considered demented: 1 with a right frontal lobe lesion, 1 with a right parietal lobe lesion and 1 with a right temporo-parietal lesion. Two patients with left temporo-parietal lesions were considered severely aphasic, and 1 patient with a left frontal lobe lesion was considered both severely aphasic and demented on the basis of neurological examination.

Thirty-five patients were originally tested: 28 with gliomas, 5 with solitary metastases and 2 with meningiomas. Diagnosis and localization were made by a neurologist, based on neurological, radiological and neurosurgical evidence. Lesions were classified as either frontal or posterior, based on the locafization of tumor anterior or pasterior to the Rolandic fissure, with temporal lobe tumors included in the posterior group. There were two subjects (one with a left-frontal glioma, one with a right-posterror glioma) who were unable to complete testing. One left-frontal glioma patient completed testing but was subsequently determined to have additional diffuse tissue necrosis, based on pathological and CT evidence. The data from these three subjects are not included in the analyses.

The remaining 32 subjects constituted 4 groups, based on the location of the lesions: 10 left-frontal (LF), 10 right-frontal (RF), 6 left-posterior (LP) and 6 right-posterior (RP). Within the posterior groups, there were 5

EFFECTS OF FRONTAL LOBE LESIONS 515

patients with parietal lobe lesions (2L, 3R), 2 patients with temporal lobe lesions (lL, lR), 3 patients with temporo-parietal lesions (2L, 1R) and 2 patients with occipito-parietal lesions (lL, 1R). Within the frontal groups the lesions commonly appeared to involve some combination of lateral, inferior and medial aspects, with extensive white matter involvement.

The frontal and posterior groups did not differ significantly on mean age, education, time since surgery or WAIS scores (Table 1). Included in the frontal group were 12 males and 8 females, while 5 males and 7 females comprised the posterior group. The difference in male/female composition between groups was not statistically significant (x2 =0.41, df= 1). Two patients were left-handed (lLF, 1RF) and the remainder were right-handed. Five of the 6 LP patients and 4 of the LF patients were clinically diagnosed as mild or moderately aphasic, although all had moderately good language comprehension. One right-handed woman in the RF group was also considered aphasic, primarily due to mildly dysfluent speech and word-finding difficulties.

Table 1. Subject characteristics

Group Age Education Chronicity’ WAlSt

n (yr) (yr) (months) Sim. Bl. Des.

Frontal

Posterior

1 20 43.1 14.1 10.6 8.81 s.d. (10.5) (2.2) (1::;) (2.5) (2.4) 2 12 40.7 15.3 4.2 12.3 9.4

s.d. (11.7) (1.4) (5.5) (2.5) (4.6)

*Since surgery. tAge-corrected scale score. $n= 15.

Procedure Conceptformntion. This was tested using a modification of LEVINE’S [ 173 procedure. Subjects were given a series of

2-choice simultaneous visual discrimination problems, with stimuli varying on 4 binary dimensions (color, form, size and position). The stimuli consisted of different colored, upper-case letters (EZ letters), either 1.3 or 2.6 cm high, which appeared 5.2 cm apart on a white 7.8 x 13 cm card. There were, therefore, 8 possiblecues represented on each trial (e.g. large and small, red and blue, X and T, left and right). Two sets offour internally orthogonal pairs of stimuli were used: one set for trials on which the subject received reinforcement (outcome trials) and the other set for blocks of trials without reinforcement (blank-probe trials). A representative set of stimuli is shown in Fig. 1.

LEFT x

8

l

l

0

Ii

I BLACI( .ARGE STIMULI -__

b Tt

WALL

H _

YHITE T llGHT __-

FIG 1. A representative set of stimuli and the 8 response patterns which correspond to use of hypotheses by subjects. Each of the columns with filled circles represents a single hypothesis. The left or right position of the filled circle within each column indicates the corresponding stimulus

associated with that hypothesis.

516 KEITH D. CIC’ERONE, RONALD M. LATAR and Wn.r IAM R. SHAPIRO

Subjects received four 16-trial problems, each having as the correct solution a cue from one of the four dimensions (red, T, large and right, respectively). They were instructed to point to one stimulus on each trial and, from being told “correct” or “wrong”. try to discover which of the 8 cues was the solution to each problem. On the first training problem subjects received verbal reinforcement after each trla!, while on the remaining problems there were only 4 outcome trials (as described below). After each training problem the subject was asked to identify the solution verbally. and any subject who could not do so was given the same problem again. If a subject still failed to solve the problem on the second attempt, he or she was told the solution and then attempted to solve the next problem. .4 subject had to solve at least 2 of the training problems in order to be given the experimental problems.

Eight 16-trial test problems were admimstered, with no verbal responses required ofsubjects. Subjects pointed to one stimulus on each trial; they were told either “correct” or “wrong” after trials 1,h. 1 I and 16 (the outcome trials). The nature of feedback on the first 3 outcome trials on each problem was predetermined and independent of the subject’s response. Each of the 8 possible combmations of”correct wrong” which can occur on 3 trials was assigned to one problem. On the remaining 12 blank-probe trials of each problem the other set of stimuli were presented in systematically varied order. The subject’s pattern of responding on each sequence of4 consecutive blank-probe trials was used to define the hypothesis held by the subject, if any, smce there is a umque pattern of respondmg which corresponds to each of the 8 cue-selection rules (see Fig. I !. There were, therefore. 3 hypotheses inferred from each ol the 8 problems, so that a total number of 24 hypotheses could be used by a subject. On the 16th trial the subject was told “correct” on half the problems, and nothing was said on the other half.

An ugpropriute hypothesis was defined as one of the logically correct hypotheses remaining after each outcome trla!. The use of appropriate hypotheses was determined separately for each hypothesis-sequence (Hl. H2 and tl?) after either a positive or negative outcome trial. This method of analysis resulted in 6 conditions, with 4 hypothesis-probes under each condition. for each subject. A correct solution was defined as the use of an appropriate hypothesis on H3 together with acorrect response on trial 16; thus there was acriterion of 5 correct responses on the last 5 trials of each problem.

hrwuiontri analysis. Twenty-four subjects (16 with frontal lobe lesions and 8 \*ith posterior lesions) were also tested on visual discrimination transfer after they had completed the testing for concept formation, using a procedure adapted from OSCAR-BERM&N and SAMcrr1.s [ZS]. The purpose of this task was to assess the subjects’ ablllty to attend to relevant stimulus dimensions and to examine the effects of positive and negative feedback. TheI-e were six Stria! transfer problems. ‘The first trial of each problem consisted of a pair of 4-dimensional stimuli similar to those used for concept formatlon. The subject had to choozc one stimulus and was told either “correct” 01. “incorrect” in predetermined order. On each of the subsequent four trial:: only one of the relevant stimulus dimensions was represented and the other three were collapsed (e.g. a lurye and a ,~~all black square in \,ertica! array), and subjects were tested for transfer of the correct response on each dimension

Testing was always conducted in a single session. which typically lasted 1: ’ 2 hr. The training and experiment&i hypothesis-sampling problems required 60 90 min. with an additional 30 min required for the discrimination transfer problems.

RESULTS

Data were subjected to a 2 x 2 ANOVA of unweighted means [ 141 comparing hemisphere of lesion and frontal/posterior locus. Subsequent analyses were conducted with two-tailed I tests unless otherwise indicated.

Hypothesis sampling

Subjects with frontal lobe lesions attained fewer correct solutions (F= 10.70, Ilf‘= 1. 28. P~0.01) and used fewer appropriate hypotheses (HA) (F= 15.84, df’= 1, 28, P<O.OOl) than subjects with posteriorly situated lesions, although there was no difference in the total number of hypotheses (H) used (F= 1.80, dj'= 1, 28) (see Fig. 2). There were no significant effects of hemisphere of lesion on correct solutions (F- 1.03, (I’l’= 1. 28), number of HA (F= 1.25. @= 1, 28) or total number of H used (F=O.23, df’= 1.28); nor were the hemisphere x frontal/posterior interactions significant for any of the above measures.

The number of HA used by subjects on each of the three H-sequences following either a positive or negative outcome trial is shown in Table 2. Subjects with frontal lobe lesions used significantly fewer HA following negative than positive outcome trials on HZ (dependent t = 3.12, df== 19, P ~0.01) and on H3 (t = 3.62, !I’= 19, P~0.01). The difference between HA following positive or negative outcome is not significant for the subjects with posterior

EFFECTS OF FRONTAL LOBE LESIONS 517

I 100 - T T 1

90 I 80 -

II LF d RF LP RP ,, TOTAL APPROPRIATE

SOLUTIONS HYPOTHESES HYPOTHESES

FIG 2. Mean percentage of correct solutions, total hypotheses used and appropriate hypotheses used during concept formation by left frontal (LF), right frontal (RF), left posterior (LP), and right

posterior (RP) subjects. Brackets indicate+ 1 sd.

lesions on any H sequence. Compared to the subjects with posterior lesions, subjects with frontal lobe lesions were significantly impaired in their ability to eliminate irrelevant hypotheses following a negative outcome on all H-sequences (Table 2). The subjects with frontal lobe lesions were also impaired in the selection of an appropriate hypothesis on H3, even after a positive outcome (Table 2). These subjects, therefore, may make less efficient use of prior information on H3 since there is an increasing likelihood over successive trials that a positive outcome will have been preceded by at least one negative outcome trial.

The ability of subjects to “focus” systematically on an appropriate hypothesis over

successive trials is represented in Fig. 3 as group&using scores. Each focusing score is a measure of the agreement between the number of logically appropriate hypotheses on a given H-sequence and the proportion of appropriate hypotheses actually used by subjects (see [17]). Since the effect of an outcome trial (either positive or negative) is to reduce the number of logically remaining hypotheses by half, the number of appropriate hypotheses for the first sequence (Hl) is equal to 4, for the second sequence (H2) is equal to 2, and for the third

Table 2. Mean number of approprtate hypotheses (maximum four) on Hl, H2 and H3 following either positive or negative outcome trials (two-tailed t tests following ANOVA)

Positive outcome Negative outcome Hl H2 H3 Hl H2 H3

Frontal

Posterior

x 3.20 3.05 1.95** 2.35** 1.05** 0.50; s.d. (0.70) (0.76) (0.76) (1.23) (0.94) (0.76) x 3.25 3.50 3.00 3.25 2.33 1.17

s.d. (0.87) (0.67) (1.04) (0.75) (1.15) (0.94)

An appropriate hypothesis was defined by the use of an hypothesis consistent with all prior feedback Difference between groups significant at: *P<O.O5; **P <O.Ol.

518 KEITH D. CICERONE, RONALD M. LAZAR and WILLIAM R. SHAPIRO

LL F: FRONTAL 1 -

“‘-0 P-POSITIVE P:POSTERIOR

I I I

( ‘$3, [ !B$S) [!?l]

TRIAL SEQUENCES

FIG. 3. Group focusing scores for frontal (circles) and posterior (squares) subjects for each of the hypothesis probes following negative (solid lines) or positive (broken lines) outcome trials.

sequence (H3) is equal to 1. Perfect focusing will, therefore, result in scores of 4.0,2.0 and 1.0 on trial sequences Hl, H2, and H3 respectively; higher scores indicate less efficient focusing. The performance of subjects with frontal lobe lesions following negative outcomes (F-negative curve) became progressively worse from Hl to H2 (dependent t = 3.73, dJ= 19, P<O.OOl) and from H 1 to H3 (t = 7.28, df= 19, P< O.OOOl), suggesting that they became less efficient in their ability to eliminate irrelevant hypotheses on successive trials.

Stimulus prejerences

The frequency with which subjects chose color, form and size hypotheses was distributed fairly evenly for both frontal and posterior groups (32,25 and 32 “/, of total H for all subjects).

Position hypotheses were least preferred by both the frontal (7%) and posterior (1896) groups; comparison of dimension preferences between groups approached significance only for the use of the position cue (t = 2.38, df’= 30, P < 0.10, Dunn’s test). Dimension preferences on the first sequence of blank-probe trials (Hl), when all four dimensions were still logically possible solutions, showed a similar pattern.

Cognitive strategies

The total number of win-stay and lose-shift strategies differed between subjects with frontal lobe or posterior lesions (F =4.26, df‘= 1, 28, P ~0.05). Furthermore, this difference could be attributed to the difficulty of subjects with frontal lobe lesions in shifting from an hypothesis which produced negative feedback (t =2.44, df= 30, P~0.05, Dunn’s test). although they were able to maintain an hypothesis following positive feedback as well as the subjects with posterior lesions (t = 1.01, df= 30, P>O.30) (Fig. 4).

Strategic errors were more common following negative than positive outcomes for both groups, although the difference was significant only for subjects with frontal lobe tumors (dependent t = 2.74, df = 19, P < 0.05).

A win-shift error was scored when a subject demonstrating an hypothesis on a sequence of blank-probe trials was told “correct” and then shifted to either a new hypothesis or no hypothesis on the following H-probe. There was no difference between frontal and posterior groups in the mean number of win-shift errors (F=0.06, df= 1, 28) (Table 3).

EFFECTS OF FRONTAL LOBE LESIONS 519

100

90

SO

70

z a =O

z 50

0” u 4o ul 0 30

20

10

WIN- LOSE- STAY SHIFT

-

RESPONSE STRATEGY

FIG 4. Mean percentages of appropriate strategies used after positive (winstay) or negative (lose-shift) outcome trials. Frontal subjects represented by dark bars, posterior subjects by light bars.

*Frontal group differs from posterior group at P<O.O5.

Table 3. Mean number and (range) of processing errors

Group n Win-shift Lose-O Lose-stay

Frontal Perseverative 8 0.8

(@;)

(O-4)

(& 0.8

(O-2)

0.3

(O-l) 2.0

(O-8) 0.6

(0-l)

Lose-O errors were scored when the subject used an hypothesis which was designated as “wrong” on the subsequent outcome trial and then failed to use any hypothesis on the following H-probe. The mean number of lose-0 errors did not differ between groups (F =0.99, df= 1, 28).

The incidence of lose-stay errors (i.e. when the subject continued to use the same hypothesis despite being informed that it was incorrect) was greater for the subjects with frontal lobe tumors and accounted for nearly half (49%) of their total errors. The difference in mean lose-stay errors between the frontal lobe and posterior groups just failed to reach significance (F = 3.67, df = 1,28, P < 0.066); this appeared to be due to significantly greater variability within the frontal lobe group (F ratio = 24.23, P < 0.0001). We observed, however, that none of the subjects with posterior lesions made more than one lose-stay error, while 40% of the subjects with frontal lobe lesions (5LF, 3RF) made two or more errors of this type. This difference is significant by the Fisher Exact Test (P=O.O12).

520 KEITH D. CICERONE, RONAID M. LAZAR and WIIUIAM R. SHAPIRO

Since not all subjects with frontal lobe lesions exhibited a dominant perseverative error tendency, hypothesis sampling was re-examined to compare frontal-perseverative* (Fp) and frontal-non-perseverative (Fnp) subjects. Fp subjects used significantly fewer HA than the Fnp subjects (t = 3.63, df= 18, P ~0.01, Dunn’s test), while the Fnp subjects remained inferior to the subjects with posterior lesions (t = 2.42, elf= 22, P ~0.05, Dunn’s test). There were no significant differences between the Fnp and posterior groups in the use of appropriate cognitive strategies (i.e. win-stay+lose-shift: t = 1.17, df=22) or the occurrence of errors other than lose-stay (f =0.7’8, df=22) (see Table 3).

Although there were no differences between left and right hemisphere lesion groups on measures of hypothesis sampling, it remained possible that they were performing at equivalent levels but still making qualitatively different types of errors. However, we failed to detect a difference between the left and right hemisphere groups on win shift errors (F = 0.25, df= 1, 28), lose-0 errors (F =0.08, df= 1, 28) or loseestay errors (F= 1.09, &= 1, 28).

Dimensional analysis

The results of discrimination transfer testing were consistent with the findings from hypothesis sampling: frontal lobe lesions produced greater impairment than posterior lesions (F=6.39, df= 1, 20, P <0.05), with no difference between left and right hemisphere lesions (F= 1.54, df= 1,20). Based on the pattern of errors during hypothesis sampling, the results of discrimination transfer were assessed separately for Fp, Fnp and posterior (P) subjects. Table 4 shows that Fp subjects made significantly more errors than both the Fnp and P subjects, with no difference between the latter two groups. Although the Fp group was impaired on all transfer measures, errors across stimulus dimensions, preferred vs non-preferred dimensions,? positive vs negative outcomes and early vs late transfer trials were similar for all groups (Table 4, difference scores).

Injluence of aphasia, age and chronicit

There was no difference between left hemisphere aphasic and left hemisphere non-aphasic subjects in the number of HA used (t =0.91, df‘= 14) or number of loseestay errors (t =0.30, df= 14) during hypothesis sampling.

Among the subjects with frontal lobe lesions increased age was significantly associated with fewer HA (Pearson r= -0.49. cif= 18, P~0.05) and more lose-stay errors (r=0.58, df= 18, P<O.Ol). Neither HA nor lose-stay behavior was related to age in the posterior group. There was no correlation between time since surgery and hypothesis sampling for any subject group.

DISCUSSION

The interpretation of brain-behavior relationships in subjects with cerebral neoplasms is frequently complicated by non-focal, pathophysiological effects of the disease process (e.g. edema, increased intracranial pressure, mass effects and necrosis) which tend to obscure

*A perseverative subject was defined as any subject making 2 or more lose-stay errors during hypothesis samplmg (i.e. > .F = 1.5).

t“Preferred” refers to each subject’s two most frequently used dimensions during hypothesis sampling, with the remaining two designated “non-preferred”.

Tab

le

4. M

ean

erro

rs

on

disc

rim

mat

ion

tran

sfer

Gro

up

Tot

al

erro

r D

imen

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s*

Out

com

es

Tra

nsfe

r tr

ials

n sc

ore

Pr.

NPr

. D

iff.

+

_ D

iff.

1+

2 3+

4 D

iff.

k7

!

Fron

tal-

pers

ever

ativ

e (F

p)

8 8.

1 4.

6 3.

5 1.

1 4.

1 4.

0 0.

1 3.

3 4.

8 -1

.6

si

Fron

tal-

non-

pers

ever

ativ

e (F

np)

8 1.

6 1.

1 0.

5 0.

6 0.

6 1.

0 -0

.4

0.4

1.2

-0.8

a

Post

erio

r (P

) 8

0.8

0.6

0.2

0.4

0.4

0.4

0.0

0.2

0.6

-0.4

P :

Sign

ific

ance

le

vel

of g

roup

co

mpa

riso

ns

S Fp

vs

Fnp

0.

005

0.00

5 0.

005

n.s.

0.

005

0.01

n.

s.

0.05

0.

01

ns.

I Fp

vs

P

0.00

1 0.

001

0.00

1 n.

s.

0.00

5 0.

005

n.s.

0.

01

0.00

5 n.

s.

Fnp

vs P

6

n.s.

0 2

*Pr.

= p

refe

rred

di

men

sion

s:

the

tvvo

dim

ensi

ons

used

m

ost

freq

uent

ly

by

a su

bjec

t du

ring

hy

poth

esis

sa

mpl

ing;

N

Pr.

= no

n-pr

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red

dim

ensi

ons;

D

iff.

= d

iffe

renc

e.

522 KEITH D. CICERONE, RONALD M. LAZAR and WILLIAM R. SHAPIRO

differences related to the regional location of the tumor. Despite these factors, the results suggest that it is possible to differentiate the effects of localized anterior and posterior cerebral tumors on a measure of complex discrimination learning.

The data show that subjects with unilateral tumors of the frontal lobe are impaired on a measure of general concept formation (number of‘correct solutions) compared to subjects with tumors confined to the posterior hemisphere. The evidence also indicates that subjects with either anteriorly or posteriorly situated lesions utilize hypotheses at the outset of discrimination learning and are able to maintain a positively reinforced hypothesis, suggesting that these two cerebral regions are equipotent for this aspect of the task. While there were no non-brain-damaged subjects run in this study, the subjects with posterior lesions generally appeared to perform at a level comparable to normal subjects, based on the pertinent data available in the literature [17, 27, 361.

The nature of the frontal lobe deficit is most apparent in the use of fewer hypotheses over the course of concept formation, and especially in the failure to eliminate an irrelevant hypothesis (focusing) despite being informed that it is incorrect. Evaluation of subjects’ cognitive strategies also suggests that the subjects with frontal lobe tumors have difficulty in responding appropriately, following negative feedback, with a lose-shift strategy. Lose-stay (i.e. perseverative) errors occurred with greater frequency among the subjects with frontal lobe tumors, while there were no differences in non-perseverative errors, consistent with the findings of MILNER [22] and DREWE [9] on the WCST. These results suggest that the subjects with frontal lobe lesions may be less sensitive to, or less able to utilize, the effects of a negative outcome.

Although, in quantitative terms, positive and negative outcome trials provide equivalent information, they produce different processing demands on the subject. When told “correct” the subject may directly encode the stimulus without further analyses, and automatically maintain the selected hypothesis. On being told “wrong” the subject must reclassify those properties of the stimulus as irrelevant, and perhaps resample the results of previous outcome trials, in order to select a complementary appropriate hypothesis. According to LEVINE [17].

the need for additional stimulus processing following negative reinforcement produces three disadvantages to the subject: additional time is required; there may be interference from irrelevant properties of the originally chosen stimulus; and the subject may fail to encode all of the relevant stimulus properties. Research on the types of error committed following a negative outcome trial has also indicated that subjects may not only fail to eliminate an irrelevant hypothesis but are equally likely to omit one or more appropriate hypotheses from consideration [4, 151. Observation of our subjects during problem-solving, primarily their spontaneous verbalizations following outcome trials, suggested to us that they had difficulty in simultaneously analyzing multiple attributes of the stimulus and were restricting the size of their hypothesis set. The results of discrimination transfer testing also suggest that the subjects with frontal lobe lesions, particularly those for whom perseveration was the dominant error tendency, were failing to attend to all of the relevant aspects of the informing stimuli. Thus the underlying deficiency of the subjects with frontal lobe lesions. on both hypothesis sampling and discrimination transfer, may be related to an attentional-control process which monitors feedback from the environment and segregates relevant from irrelevant sources of information (see also [19. 20, 33, 34.381).

This interpretation of the frontal lobe deficit is also compatible with the observation that frontal lobe lesions produce difficulty in suppressing inappropriate hypotheses acquired over the initial course of learning [7,24,25,29,39]. That is, attending only to restricted aspects of

EFFECTS OF FRONTAL LOBE LESIONS 523

the stimulus will reduce the probability of learning an alternative cue-response association and increase the likelihood of repetitive responding. We therefore consider the impairment of attentional selectivity and an increased perseverative tendency to be related aspects of the frontal lobe disturbance.

Acknowledgements -This research was supported in part by Biomedical Research Support Grant No. RR 05753-09 to Memorial Hospital. We would like to thank DORIS PENMAN for her continuing assistance with this work, JEROME B. POSNER, MAX POLLACK and PHILLIP RAMSEY for their suggestions, and ALEON PRATT for her helpful comments on the manuscript.

1

2

8

9

10

II.

12.

13.

14. 15

16.

17. 18. 19.

20.

21.

22. 23.

24.

25.

26. 27.

28.

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32 sujets poreeurs de tumeurs c&rdbrales unilatBrales ant 6t6 test&s sur l’utilisation d’hypoth2ses et de strategies cognitives au co”,-s d’une tPche de discriminatton visuelle. Les sujets porteurs d’une lesion du lobe frontal parviennent 2 un nomhre mains 61~6 de concepts et utilisent mains d’hypothPses correctes que les sujets atteints de tumeurs hemispheriques post6rieures, bien que le nombre total d’hypotheses utflisees soit le m8me. La persCveration d’erreurs s’est retrouGe a”ec une fr6quence plus BlevGe parmi les malades avec Xsions frontales, sans que tous les sujets de cette cat6gorie presentent cette tendance. Les resu1tats CO”cer”a”t la selection d’hypotheses ainsi q”‘lI”e seconde tlche de transfert de discrimination visuelle, suggerent que le deficit lie aux Esions frontales correspond 1 une difficult6 a integrer des indices multiples et B prendre en rompte le feedback pour s6lectlonner les sources d’information appropriges.

Zusammenfassung:

32 Personen mit einseitigen Hirntumoren wurden auf ihre Hypothesen und cognitiven Strategien wzhrend einer vi- suellen Unterscheidungsaufgabe untersucht. Personen wit FrontallappenschSdigungen entwickelten weniqer Konzeote und benutzten weniger geeignete Hypothesen als Patienten mit Tumoren, die im rtickwlrtigen Anteil des CroBhirns lokalisiert ware", obwohl sich kein Unterschied in der Gesamtzahl der Hypothesen ergab. Ein Fehlertyp, bei dem die Versuchsoersonen vom ffalschenl Eraebnis der voran- gehenden Lssbng nicht proiitierten; wurde mit grtil3erer H;iufigkeit bei P 'atienten mit FrontallappenlBsionen be- obachtet. obwohl dieser Fehler nicht van allen Frontal- laooenoatienten gemacht wurde. Die Ergebnisse des Hypo- theienbrdnens und einer zweiten Aufqabe fUr den Transfer van visuellen Unterscheidungsleistuigen schienen zu zei- qen. daO der Leistunqsmanqel durch SchB'diounq des Fron- ialliirns zu Schwierigkeiten in Beziehung ;tand, verschie- denartige Schltisselreize zu beachten und Rfickmeldungen zu verarbeiten, um wichtige van unwichtigen Informationen voneinander zu trennen.