Neurop,ychologia, Vol. 23, No 3, pp. 371 379, 1985. Prmted I” Great Brltam

C028-3932/85 $3.00+0.00 C, 1985 Pergamon Press Ltd.

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY-II. THE SYNTHESIS OF PHONEMIC AND

SEMANTIC INFORMATION

LAURIE MILLER and BRENDA MILNER

Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, Quebec, Canada. H3A 2B4

(Accepted 31 October 1984)

Abstract-Patients with unilateral cerebral excisions and control subjects performed two tasks in which target words had to be guessed on the basis of either phonemic or semantic partial-information clues. Each cumulatively provided clue was assigned successively lower point-value, these points being risked whenever the subject responded. Patients with frontal-lobe excisions chose to make a guess after seeing only one clue more often than did a combined group of subjects without frontal-lobe damage, but this guessing-score was also related to extent of right temporal-lobe removal. Patients with left temporal-lobe or left frontal-lobe lesions had difficulty solving the verbal clues, occasionally failing to recognize that a response generated in the context of one clue satisfied all the clues.

INTRODUCTION

THIS EXPERIMENT parallels one in which impulsive guessing on a visual task was demonstrated in patients with right fronto-temporal excisions and, to a lesser degree, in patients with left or right frontal-lobe excisions (see MILLER [lo], this issue). We were interested in investigating whether such behaviour would manifest itself also on verbal tasks that again allowed subjects to choose to guess target items after seeing either one, two, or all three clues of a set, but that required the use of either phonemic or semantic clues rather than fragmented line-drawings. By thus varying the task material, it was possible to determine (1) whether there would be material-specific effects on guessing behaviour (possibly related to the side of cerebral excision), and (2) whether, within each clinical group, individuals would maintain consistent strategies across different tasks.

In addition to providing a measure of risk-taking (the number of first-card guesses), these experimental tasks assessed the ability of subjects to integrate the information contained in the clues. It was predicted that patients with frontal-lobe lesions would be impaired in this ability, since there are clinical reports showing that, after extensive frontal-lobe damage, patients tend to misunderstand proverbs and metaphors because they use only fragments of the text (ZEIGARNIK cited by [S], [24]). Patients with left temporal-lobe lesions were also expected to be poor at combining the verbal clues because oftheir known difficulty in holding and manipulating verbally expressed ideas [9, 11-13, 16, 223.

A second skill that may facilitate the identification of target words is the ability to generate several possible responses for each clue. It is well established that patients with left frontal- lobe lesions have low verbal fluency when asked to think of as many words as possible beginning with a specified letter within a limited time [2, 14,19,20]. It has also been found that patients with left temporal-lobe lesions are impaired when asked to generate, under a time

371

312 LAURIE MILLER and BRENDA MILNER

constraint, rhymes or synonyms [21], or nouns belonging to specific semantic categories ([17], MILNER, unpublished data, 1983). For these various reasons, it was predicted that

patients with left frontal-lobe or left temporal-lobe removals would be poor at identifying target words. Patients with removals from the right hemisphere were not expected to have

any difficulty on these verbal tasks.

METHOD

Subjects Forty-four patients who had undergone elective surgery for the relief of epilepsy, as well as 23 normal control

subjects (NC) matched to the patient population on the basis of sex, age, and level of education, were included in this study. Only subjects who spoke English as a first language performed the verbal tasks. Table 1 shows the Full-Scale IQ data for the patients. subdivided according to site and side of cortical excision, as well as the sex, age, and

Table 1. Subjects

Group

Age Education Sex (yr) (yr) Weschsler IQ

MF Mean Range Mean Range Mean Range

Normal control Right temporal Left temporal Right frontal Left frontal Right fronto-temporal

9 14 29.1 17 -49 14.2 11 18 not assessed 3 8 27.5 17-48 13.6 lo- 18 112 91-131 9 9 25.1 16 39 13.2 9-18 106 86-127 5 I 34.5 20 -47 12.2 7-21 105 877116 3 0 25.0 13 37 10.3 8 12 102 97 -106 3 3 28.5 21~36 15.2 13-18 104 93-l 19

educational level for all subject groups. Twenty-one patients were tested between two and three weeks after operation, and 18 were seen one or more yr after surgery. Because no relationship was found between the size of hippocampal removal and performance on either task, patients with either large or small hippocampal excisions were combined to form the temporal-lobe groups in this report. MILLER [lOI describes in more detail the population from which these patients were drawn and includes brain maps for the patients with frontal-lobe excisions.

Right temporal-lobe group (RT). For the 11 patients with right temporal-lobe excisions, the mean extent of removal was 4.8 cm along the Sylvian fissure and 5.9 cm along the base of the brain.

hfi temporal-lobe group (LT). The 18 patients with left temporal-lobe excisions had removals that averaged 4.1 cm along the Syivian fissure and 4.9 cm along the base of the brain.

Right frontal-lobe group (RF). There were six patients with right frontal-lobe removals, including two with excisions limited to the lateral surface (Da. Co., Ke. MC.), one with a dorsolateral lesion that extended medially to include part of the cingulate gyrus (El. Ke.), and three with large removals involving lateral, orbital, and medial surfaces (Da. Ya, Ch. Ma., Jo. Ed.).

L&Ji-ontal-lobe group (LF). Of the three patients in the left frontal-lobe group, one had an excision involving the dorsolateral surface and the medial surface down as far as the corpus callosum (To. Fa.). and the other two had excisions that also invaded the ventrolateral and orbital surfaces (Hu. Ma., Th. Fe.).

Righr Jionto-temporal group (RFT). This group consisted of six patients who had temporal-lobe removals that extended an average of 5.2 cm along the Sylvian fissure and 6.2 cm along the base of the brain, in addition to relatively limited removals from the right frontal lobe.

Stimuli

The test material for each of the two verbal tasks comprised 17 sets of cards. The three cards of a set provided clues about a target item, the identity of which the subject had to guess. Both tasks were designed so that it was highly unlikely that subjects would guess the target item correctly on the basis of the first clue. Adding the second clue narrowed down the number of possible solutions without limiting the subject to only one obvious choice. The third clue was meant to facilitate greatly the generation of the target word. In all sets, only one word fit all three clues.

Phonemic Task. Typewritten clues referring to phonemic aspects of target words appeared on the cards used in this task. The first clue of a set supplied a rhyme having the same number of syllables as the target. The second clue concerned the spelling of the target word, and the third stated the first letter of that word. Target items were selected

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY--II 373

Table 2. Sample clues taken from the two verbal tasks

Phonemic Task Semantic Task

1 Rhymes with flower Means “got up” Clues 2 Has four letters A well-known type of flower

3 Begins with an “s” A shade of red Target item sour rose

on the basis of having (1) several possible rhymes, and (2) a phonemic element that could be expressed using different letter combinations. The first column in Table 2 shows a representative set of phonemic clues.

Semantic Task. Each clue in this task provided information about a different semantic context in which a target word could be used. The target items were homonyms having at least three definitions (see the second column in Table 2 for a sample set of clues taken from the Semantic Task).

Procedure

Before each task, the nature of the clues was described and illustrated with an example. Cards ofeach set were then presented cumulatively and subjects were free to guess the target word after seeing either one, two, or all three cards. Table 3 shows the number of points that could be won or lost with a guess after seeing the first, second, or third card, respectively. The number of guesses made after only one card had been shown was taken as an indication of risk- taking.

Table 3. Point-scoring system

Number of cards presented

Number of points won Correct guess Incorrect guess

1 + 50 - 50 2 +30 -30 3 +5 - 5

The subject’s ability to combine information provided on the cards, thereby arriving at the correct response, was also measured. In those instances where the subject had guessed incorrectly before having seen all three cards of a set, the remaining cards were displayed and, with no points involved, the subject was asked to guess the item a second time. During a pilot study, this step was occasionally found to result in subjects voicing the target word in response to a particular clue on the Semantic Task, without realizing that the spoken word was the correct answer. Therefore, during the actual experiment, if subjects were unable to produce the target word after seeing all three semantic clues, they were asked to generate responses that applied to each individual clue. In this way the subject’s ability to recognize a word generated in a particular context as applicable to all the clues was assessed.

RESULTS

The three main measures used to assess perormance on these verbal tasks were the same as those used on the visual tasks (see MILLER [lo]). These were: (1) a risk-taking score (the number of first-card guesses); (2) a synthesizing-ability score (the number of items eventually answered correctly, with an item being counted if either a subject’s first guess was correct, or, after an initial wrong guess, the subject gave the correct answer when shown all three cards); (3) two incorrect-response scores (the number of times a response was given that did not satisfy all the information provided on the cards, and the number of times correct answers were generated but not recognized as satisfying all the clues). In addition to these measures, group-differences in the mean number of points won were analyzed.

314 LAURIE MILLER and BRENDA MILNER

In the one-way analyses of variance that follow, the LF group was not included because it consisted of only three subjects. This group was involved, however, in those planned comparisons that combined the scores of all patients with frontal-lobe lesions and compared them to the combined scores obtained by the remaining groups.

Risk-tuking

The prediction that patients with frontal-lobe lesions would make more first-card guesses than other subjects was tested with planned comparisons, which revealed that on both tasks the mean risk-taking scores of a combined group of patients with frontal-lobe excisions were significantly higher than the combined scores of normal control subjects and patients with temporal-lobe lesions [Phonemic Task (following a log transformation) : F = 4.88, P < 0.05; Semantic Task: F = 7.18, P < 0.011. Table 4 gives the mean number of first-card guesses made by each group.

Table 4. Risk-taking: mean number of first-card guesses (maximum= 17)

Task Normal control

Right temporal

Group Left Right Left Right fronto-

temporal frontal frontal temporal

Phonemic 1.5 4. I 1.9 4.2* 5.0* 1.7* Semantic 2.8 4.2 1.6 4.5t 7.0t 6.3t

*tCombined right frontal-lobe, left frontal-lobe and right fronto-temporal groups differ from normal control, right temporal-lobe and left temporal-lobe groups combined (P<O.O5).

No correlations were found between the number of first-card guesses and the extent of frontal-lobe or left temporal-lobe removal; in contrast, the extent of right temporal-lobe removal along the Sylvian fissure was positively correlated with the risk-taking score for both tasks (Phonemic: r = +0.60, P=O.O5; Semantic: r= +0.64, P=O.O3). The number of first-

card guesses made by the RT group, however, did not differ significantly from the number made by the NC group on either task.

On both tasks (and unlike the results of MILLER [lo]) there was a negative relationship between the number of items guessed with only one card and the number of points obtained (Phonemic Task: I’= -0.71, P=O.OOl; Semantic Task: r= -0.47, P=O.OOl). On the Phonemic Task, a one-way analysis of variance on the number of points won by each group was significant (F=2.63, P<O.O5), with the NC group obtaining the highest number of points and the RT group the fewest (see Table 5), but post hoc comparisons did not reach the 0.05 level of significance (Q=3.14; at P=O.O5, Q=3.98). On the Semantic Task, a one-way analysis of variance (F = 5.05, P~0.01) followed by Newman-Keuls post hoc tests revealed that the NC group won more points than any other group.

For each group, Pearson product-moment correlation tests were also carried out to examine the relationship between risk-taking scores on the two verbal tasks, and to compare these with the risk-taking scores obtained on a similar visual task (Visual Task With Points, see MILLER [lo]). For every group except the normal-control and left frontal-lobe groups, there was a positive correlation between the number of first-card guesses made on the two verbal tasks (RT: r= +0.93, P=O.OOl; LT: r= f0.52, P=O.O3; RF: r= +0.85, P=O.O3;

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY--II 315

Table 5. Mean number of points won

Task Normal Right control temporal

Group Left Right Left* Right fronto-

temporal frontal frontal temporal

Phonemic 45 - 130 - 56 - 109 -86 - 102 Semantic 290t 108 100 63 - 153 12

*Left frontal-lobe group not included in the ANOVAs. tNorma1 control group differs from all other groups (P~0.01).

RFT : r = + 0.81, P = 0.05). When risk-taking scores from the Visual Task With Points were compared with those from each of the verbal tasks, only the patients in the left temporal-lobe group showed any consistency, and this was only in going from the Visual Task With Points to the Phonemic Task (r = f0.54, P=O.O2).

Synthesizing ability

The ability to integrate the clues was not correlated with the number of first-card guesses but, on both tasks, this measure was positively correlated with educational level (Phonemic Task: r= +0.31, P=O.Ol; SemanticTask: r= +0.41, P=O.OOl), and, on the SemanticTask, with Verbal IQ (r = +0.49, P=O.OOl). One-way analyses of variance and post hoc tests, however, demonstrated no differences between groups with respect to either of these two variables.

Table 6 gives the mean synthesizing-ability score for each group. For both tasks, one-way analyses of variance yielded significant differences between groups (Phonemic: F = 2.95,

Table 6. Synthesizing ability: mean number of items correctly identified (maximum = 17)

Task Normal control

Right temporal

Group Left Right Left* Right fronto-

temporal frontal frontal temporal

Phonemic 16.0 15.7 14.67 15.2 10.7 14.7 Semantic 14.0 11.61 g.6# 10.71 7.7 12.2

*Left frontal-lobe group not included in the ANOVAs. tLeft temporal-lobe group differs from the normal control group (P-cO.05). fRight temporal-lobe and right frontal-lobe groups differ from the normal control group (P~O.001). §Left temporal-lobe group differs from the normal control, right temporal-lobe and right fronto-temporal groups

(P<O.OOl).

P~0.05; Semantic: F= 11.35, P<O.OOl). Patients with left temporal-lobe lesions were impaired relative to normal control subjects on both tasks. On the Semantic Task, Newman-Keuls post hoc tests also showed that the LT group identified fewer target words than either the RT or RFT group, and that all groups except the RFT group were inferior to the NC group. On the two verbal tasks, the mean synthesizing-ability scores for the three patients in the LF group (not included in the analyses) were even lower than the means of the LT group. There was no relationship between the extent of frontal- or temporal-lobe removal and the ability to synthesize either phonemic or semantic information.

376 LAURIE MILLER and BRENDA MILNER

Incorrect responses

A count was made of the number of times a subject gave a response that was not considered a potential target item, given the information available at the time the guess was made. The first two columns in Table 7 show the mean number of such errors made by each group on the Phonemic and Semantic Tasks, respectively, but one-way analyses of variance revealed no significant differences between groups for either task.

Table 7. Mean error scores on verbal tasks

Group

Answers not satisfying all given information

Phonemic Task Semantic Task

Items generated but not recognized Semantic Task

Normal control 1.22 0.48 0.35 Right temporal 1.27 1 .oo 0.91 Left temporal 2.24 1.67 1.28* Right frontal 1.50 1.83 0.67 Left frontalt 1.67 2.00 2.33 Right fronto-temporal 1.83 1.67 0.67

*Left temporal-lobe group differs from the normal control group (P~0.05) tLeft frontal-lobe group not included in the ANOVAs.

Between-group differences were evident (F =2.99, P-cO.05) when an analysis was performed on the number of times a target word was generated as a possible response to a single clue without being recognized as the correct answer to the set. Patients in the left temporal-lobe group made more errors of this kind than did normal control subjects, as shown by a Newman-Keuls post hoc test (see the third column in Table 7). The three patients

with left frontal-lobe lesions averaged a higher mean error score than the LT group.

DISCUSSION

On these verbal tasks, guessing an item on the basis of only one clue proved to be an unprofitable strategy in terms of the number of points won, and thus such a guess represented a greater risk than it had on the corresponding visual task [lo] where guessing on the first card was positively correlated with the points score. This difference may have been caused by the fact that many possible responses could be generated to fit the first verbal clue of a set, whereas on the visual task (in which objects had to be identified on the basis of fragmented line-drawings), fewer plausible answers wre likely to come to mind with only the first card. This change in the probability of guessing correctly with only one card may have affected in different ways the choice of strategy made by different individuals, and thus may have led to the lack of correlation between risk-taking scores on the visual and the verbal tasks. A lack of consistency across tasks has also been noted in other experimental situations in which normal subjects have been assessed using a variety of risk-taking measuies [7, 18, 26-291.

On both the Phonemic and Semantic Tasks, patients with frontal-lobe excisions averaged significantly more first-card guesses than did a combined group of normal control subjects and patients with temporal-lobe excisions. One explanation for the high number of first-card guesses made by the frontal-lobe groups is based on evidence that such patients are impaired

COGNITIVE RISK-TAKING AFTER FRONTAL OR EMPORAL LOBECTOMY--II 311

at making cognitive estimates [25] and thus may find it difficult to assess the number of responses possible for the first clue of a set. This difficulty may well have been exacerbated by the known low verbal fleuncy of patients with left frontal-lobe lesions [2,14,19,20,30], which could have caused them to underestimate the amount of risk involved in a first-card guess. In addition, it was hypothesized that impulsive tendencies [3, 5, 14, 151 would inflate the risk- taking scores of patients with frontal-lobe excisions. It seems likely that a combination of these factors was responsible for the high number of first-card guesses made by the right frontal, left frontal and right fronto-temporal groups on these tasks where the inhibition of early responses was associated with a higher points-score.

There was no clear relationship between the amount of risk-taking and the side of frontal- lobe excision, but hemispheric differences were indicated by the risk-taking performance of

patients with temporal-lobe excisions. Patients with right temporal-lobe removals engaged in a relatively high number of first-card guesses on the verbal tasks (although their mean scores did not differ from those of the normal control group). In addition, a positive correlation was found between the size of right temporal-lobe excision and the amount of risk-taking. Patients with left temporal lobectomies, in contrast, were the only individuals to maintain consistently low risk-taking scores across the different types of task material. This finding is interesting in the light of earlier observations that patients with left temporal-lobe lesions show extremecaution when tracing paths in Porteus mazes [12] or when carrying out design-fluency tasks [6].

The effect of size of excision from the right temporal lobe, together with the consistently high risk-taking scores of the right fronto-temporal group, suggest that risk-taking, as measured in this study, may be related to the extent of right-hemisphere damage. This hypothesis finds some support in the reports of GAINOTTI [4], who observed disinhibition and indifference in patients with extensive right-hemisphere lesions. The relationship, however, between Gainotti’s findings and the risk-taking demonstrated here by patients with relatively small cortical excisions from the right hemisphere is uncertain. Furthermore, the lack of correlation between size of excision from the right frontal lobe and risk-taking argues against this idea.

Results from the synthesizing-ability measure indicate that patients with left temporal- lobe removals were impaired relative to normal control subjects in the use of both phonemic and semantic clues, The fact that such a lesion has a detrimental effect on the ability to integrate verbal information lends further support to the idea that the left anterior temporal neocortex plays a role in verbal comprehension [12, 13, 221. The present results uphold previous findings suggesting that patients with left temporal-lobe excisions are impaired at evoking words either according to their sound [21] or according to a semantic context [ 173. It is noteworthy that the deficit caused by a left temporal-lobe removal in the ability to synthesize the verbal clues does not seem to be exacerbated by inclusion of part of the hippocampus in the temporal lobectomy.

The three patients with left frontal-lobe excisions obtained synthesizing-ability scores even lower than those of the left temporal-lobe group on both tasks. It is likely that both a low verbal fluency [2, 14, 19, 20, 301 and an impaired ability to synthesize verbal material (ZEIGARNIK cited by [8], [24]) caused these patients to have difficulty solving the verbal clues. Until more subjects have been tested, however, it is premature to conclude that left frontal- lobe lesions severely impair performance on these tasks.

Although the patient groups that were the least successful at identifying target words on the Semantic Task were those with left-hemisphere lesions, groups with either right

378 LAURIE MILLER and BRENDA MILNER

temporal- or right frontal-lobe lesions were also inferior to the normal control subjects. Producing a target word on this task seems to require the generation of a list of possible responses for each clue, followed by a comparison of these sets of potential solutions in order to discover the word they have in common. On the other hand, in the tasks incorporating either visual [lo] or phonemic clues, it appears that each additional clue causes a single set of possible responses to narrow progressively. This difference in the kind of processing involved may account for the fact that patients with excisions from frontal or temporal cortex of either hemisphere were deficient on the Semantic Task, whereas only certain groups showed deficits on the other tasks. The finding of a difficulty on the Semantic Task after a unilateral frontal or temporal lobectomy is similar to the results of REITAN [23], who noted an impairment in a

group of patients with heterogeneous cerebral lesions on a task that required the replacement

of a nonsense word given in the context of five different sentences (REITAN and SHIPLEY cited

by 1231). Comparing the types of errors made by different subject groups provided some insight into

why patients with left-hemisphere lesions were so poor at solving the clues on the Semantic Task. Patients with left temporal-lobe lesions were found to generate more target words without recognizing them than did normal control subjects. This result indicates that a left temporal-lobe lesion exaggerates the difficulty occasionally experienced by normal subjects in realizing that homonyms, encountered in different contexts, are the same word [l]. Because the three patients with left frontal-lobe lesions also averaged a poor score on this measure, it may be postulated tentatively that the left frontal lobe also plays a role in this kind of semantic flexibility.

Ackno~ledqements--~This work is based on a thesis submitted by Laurie Miller in September 1983 to McGill Universityln partial fulfillment of the requirements for the M.Sc. degree. The research was supported in part by a Max Bell (Open) Fellowship to Laurie Miller and in part by grant MT 2624 from the Medical Research Council of Canada to Brenda Milner. We are grateful to Dr. Theodore Rasmussen, Dr. William Feindel, and their associates at the Montreal Neurological Hospital for the opportunity to study their patients.

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