Neuropsychologia, Vol. 23, No. 3, pp. 359-369, 1985. Pnnted in Great Brhn.

0028-3932185 $3.00+0.00 i 1985 Pergamon Press Ltd.

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMYPI. THE SYNTHESIS OF FRAGMENTED VISUAL

INFORMATION

LAURIE MILLER

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 visual tasks in which target items had to be guessed on the basis of partial information. In one task, no points were at stake, but in the second, each cumulatively provided clue was assigned successively lower point- value, these points being risked whenever the subject responded. The right fronto-temporal group chose to guess more often after seeing only one clue than any other group. The right temporal-lobe group and both frontal-lobe groups were impaired at synthesizing the fragmented line-drawings, with patients in the frontal-lobe groups making the most perceptual errors.

INTRODUCTION

CLINICAL reports of patients with extensive frontal-lobe damage have emphasized the exaggerated reactivity of such patients to irrelevant stimuli, as well as the social inappropriateness of their actions [l, 3,8, 11, l&20]. In experimental settings also, patients with frontal-lobe lesions have demonstrated a lack of behavioural restraint, as indicated, for example, by a failure to inhibit reflex-like actions [7,9], by rule-breaking [4,25,26], and by the omission of the planning stage on certain cognitive tasks ([16], GADZHIEV cited by [ 181, [29]). The first goal of the present study was to explore further the conditions under which impulsive behaviour can be elicited after unilateral excisions from the frontal cortex and to provide an objective measure of such behaviour.

To achieve this end, cognitive tasks were designed in which subjects were given the opportunity to guess target items on the basis of partial-information clues. No single clue yielded enough information to define a unique item, but clues were provided successively until the subject chose to make a response. In the present experiment, fragments of the line-

drawings of objects served as the clues, whereas in a parallel study (see MILLER and MILNER

[22], the sequel to this paper), subjects were provided with semantic or phonemic information and were asked to guess a target word.

The ability to arrive at a correct response on tasks such as these appears to involve two cognitive skills, these being the ability to generate several possible answers for each clue, and the ability to combine clues effectively. Damage to the frontal lobes has been associated with low design fluency [12,34], as well as with an inability to combine into a meaningful whole all of the elements in a complex visual scene (ZEIGARNIK cited by [18], [20, 303). In addition, patients with lesions of the right temporal lobe have been found to be impaired on visual tasks requiring the perception of incompletely represented figures [ 15,21,23,24,28]. Hence, the second goal of the present experiment was to test the hypothesis that patients with

359

360 LAURIE MILLER

excisions from either the right or left frontal lobe or from the right temporal lobe would be impaired at synthesizing fragmented visual information.

METHODS

Subjects

Each of the 69 patients studied had undergone a unilateral brain operation at the Montreal Neurological Hospital, the operations being carried out for the relief of focal epilepsy. In most instances, the cause of the seizure disorder was cerebral atrophy, static in nature, dating from birth or early life; however, nine individuals with etiologies of indolent tumour were also tested. Excluded from the patient population were those patients with evidence from computerized tomography or electroencephalography of cerebral damage beyond the extent of the excision, those with IQ ratings below 80, and those known to have bilateral or right-sided speech representation, as demonstrated by preoperative intracarotid Amytal* tests [Z]. Thirty-eight patients were tested between two and three weeks after operation, and 31 were seen one or more yr after surgery. For the entire patient group, no correlation was found between performance on the tasks and time of testing; therefore, the data from patients tested early and those tested late were combined for each lesion group.

All of the temporal-lobe removals included the uncus and the amygdala, but they varied in the amount of hippocampus excised. Because no relationship was found between performance on the experimental tasks and the extent of hippocampal excision, patients with either large or small hippocampal removals were combined to form each of the temporal-lobe groups in this report.

Twenty-three normal control subjects (NC) were selected to match the patients as far as possible with respect to sex, age, and level of education. Intelligence tests were not administered to the control subjects.

The patients were subdivided into five groups according to the side and site of cortical excision. Table 1 gives the Full-Scale Wechsler IQ data for the patient groups, as well as the sex, age, and level ofeducation for all six groups.

Table 1. Subjects

Group

Age Education Sex (yr) (yr) Wechsler IQ

M F Mean Range Mean Range Mean Range

Normal control 9 14 Right temporal 9 11 Left temporal 14 11 Right frontal 8 3 Left frontal 5 2 Right fronto-temporal 3 3

29.1 17-49 14.2 1 t-18 27.4 17 -48 12.9 lo-18 27.1 16-48 13.2 9-18 34.2 20-54 11.4 7-21 26.5 13 37 11.8 8816 28.5 21-36 15.2 13-18

not assessed 110 90-131 106 833127 102 87-116 100 97-m106 104 93-l 19

Right temporal-lobe group (RT). Each of the 20 patients in this group had undergone a right anterior temporal lobectomy, the mean extent of removal along the Sylvian fissure being 5.1 cm, with a range from 3.5 to 7.5 cm. Along the base of the brain, the mean extent of removal was 6.0 cm, with a range from 3.5 to 8.5 cm.

Left temporal-lobe group (LT). The 25 patients in this group had a mean removal along the Sylvian fissure of 4.7 cm, with a range from 4.0 to 5.5 cm. The mean removal along the base of the brain was 5.4 cm, with a range from 4.0 to 6.3 cm.

Rightfrontal-lobe group (RF). Figure 1 shows the cortical excisions for the 11 patients in this group. The removals consisted of one excision from the inferior frontal gyrus (Da. Co.), one involving only the dorsolateral cortex (Ke. MC.), four excisions that included parts of dorsolateral and medial cortex (El. Ke., Je. Bi., Ro. Bo., and Gu. Vi.), and five excisions that involved orbital frontal in addition to dorsolateral and medial cortex (Da. Ya., Ma. Si., Ch. Ma., Su. Br., and Jo. Ed.).

Leftjiontal-lobe group (LF). Shown in Fig. 2 are the cortical excisions for the seven patients composing this group. The removals included five excisions that involved both dorsolateral and medial cortex (Ra. Ja., An. Co., To. Fa., An. Be., and MO. Au.), and two excisions that involved the same areas but also extended inferiorly to include the frontal pole and a portion of the orbital frontal cortex (Hu. Ma. and Th. Fe.).

*Sodium amobarbitol, Eli Lilly & Co., Indianapolis, U.S.A.

COGNITIVE RISK-TAKING AFT!% FRONTAL OR TEMPORAL LOBECTOMY--I 361

EI.Ke.

Ch.Ma.

Da.Ya.

_,’ SuBr.

FIG. I. Brain maps based on the surgeon’s drawing at the time of operation, showing the estimated medial. lateral, and ventral extent of cortical excision from the eleven patients in the RF group; only

those surfaces from which an excision was made are thustrated.

Riyhr./ionfo-fumporal qroup (RFT). For the six patients with fronto-temporal lesions (illustrated in Fig. 3) the mean size of temporal-lobe removal was 5.2 cm along the Sylvian fissure and 6.2 cm along the base. In tvvo of these cases, the frontal excision involved only cortex from the lateral surface of the lobe (Ei. MC. and Ch. Te.); in three cases, it included lateral as well as orbital frontal cortex (Li. Da., Do. Bo., and Ma. De.), and m one case, the excision also invaded the medial surface (Jo. Da.).

362 LAURIE MILLER

,F_Q. To.Fa.

‘:,_ An.Be.

,,._Hu.Ma.

/Y,JJo.Au.

,.,JJh.Fe.

FIG. 2. Brain maps indicating the estimated extent of removal for the seven patients in the LF group. Medial, lateral, and ventral surfaces are shown for all cases in which they were included in the

removal.

Stimuli

The test material for each ofthe two tasks consisted of 17 sets of three cards each. The three cards of a set provided clues about a target item, the identity of which the subject was to guess. The “cards” were actually 7.5 x 12.5 cm pieces of semi-transparent white paper on which portions of line-drawings of objects appeared. Drawings were selected from the items on the Peabody Picture Vocabulary Test that are normally identifiable by children 3 11 yr of age. A different part of one whole picture was represented on each of the three cards making up a set. The partial figures were drawn so that, if the three cards were superimposed, a complete image would be formed, as shown in Fig. 4. The detail on each card was determined by the examiner according to the following criteria. On the first card, the fragmentary information given was probably compatible with the images of many different objects, The information on the second card was intended to reduce the number of possible objects. The third card provided the remaining information necessary to form a complete picture of a specific object.

Procedure

In both tasks, the three cards of a set were presented cumulatively and in the same order for each subject. In the instructions to the subject, the nature of the clues was described and a set of clues was provided as an example. When

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY--I 363

FIG. 3. Brain maps showing the estimated extent of removal for the RFT group. Only one of these patients (Jo. Da.) had an excision that invaded the medial surface of the frontal lobe.

First Card Second Card Third Card

Target Item

FIG. 4. A sample set of fragmented visual information clues

performing the task, the subject had the opportunity to guess each target object after seeing either one, two, or all three clues, and, in this phase of the experiment, only one guess was allowed for each set. On the first task (Visual Task Without Points), subjects were told to guess the object as soon as they were reasonably sure they knew what it was. In this case, bemg incorrect was the only risk involved in guessing before seeing all three clues. For the subsequent task (Visual Task With Points), a certain number of points were assigned to a guess made after seeing one, two or three cards, respectively. Thus, 50 points were risked when a guess was made using only the first clue; that is, the subject won 50 with a correct guess and lost 50 if the guess was not the same as the target item. Thirty points could be won or lost after seeing two clues, and just five points were at stake when all three clues had been presented. If the subject did not want to guess an item even after seeing all three clues, no points were lost or gained for that set. Subjects began with zero points and were told to try to earn as many points as possible.

364 LAURIE MILLER

If a subject guessed incorrectly before seeing all three cards, the remaining cards of the set were presented and the subject was asked to guess the item again. This step, in which no points were involved, was carried out to provide a measure of a subject’s ability to process all the available information to arrive at a solution.

RESULTS

Three kinds of measures were used to assess task performance: (1) a risk-taking score, (2) a synthesizing-ability score, and (3) a score based on the plausibility of incorrect responses. The mean number of points won by each group was also examined, with the understanding that this score probably reflected the combined influence of risk-taking strategy and synthesizing ability.

Risk-taking

Initially, two different risk-taking scores were considered: the mean number of cards used to make a guess, and the number of times guesses were made on the basis of only the first card of a set. In general, the first score was less sensitive to differences between groups, although when it did yield significant group differences, these were consistent with the differences demonstrated by the second risk-taking score. For this reason, only the results obtained with the number of first-card guesses as the risk-taking score are reported.

Pearson product-moment correlation tests, collapsed across subject groups, showed that the number of guesses made on the first card was not significantly correlated with sex, level of education, language spoken, or Full-Scale IQ. Although risk-taking proved to be correlated with age on the Visual Task With Points (r = - 0.24, P.= 0.02), a one-way analysis of variance yielded no significant differences in age between the groups; therefore, any significant

between-group differences with respect to risk-taking scores are probably not attributable to differences in age. There was no significant relationship for any of the groups between the number of first-card guesses and the ability to synthesize information on the clues. In addition, no between-group differences were found on either task for the percentage of items guessed correctly on the first card (a score obtained by dividing the number of first-card guesses that were correct by the total number of first-card guesses).

A two-way (Group x Task) analysis of variance on the number of first-card guesses revealed no interaction. On the task in which points were not involved, there was no difference between groups on this score; however, with the addition of points in the second

visual task, significant between-group differences emerged (F= 3.15, P~0.01). In this case, Newman-Keuls post hoc tests revealed that the RFT group made more of these guesses than any other group. Table 2 shows that the RFT group was the only one to increase its mean number of first-card guesses between the first visual task and the second; all the other groups demonstrated some decline in this score on the Visual Task With Points.

Table 2. Risk-taking: mean number of first-card guesses (maximum = 17)

Task

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

Visual Task Without Points 4.9 4.9 5.2 6.7 5.1 6.3 Visual Task With Points 3.2 4.1 4.6 4.8 3.3 7.7*

*Right fronto-temporal group differs from all other groups (PiO.05)

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY~I 365

A planned comparison was carried out contrasting patients with frontal-lobe lesions to a combined group of normal control subjects and patients with temporal-lobe lesions. This

comparison yielded a significant difference (F = 4.16, P < 0.05); however, as can be seen from Table 2, the number of first-card guesses made by the right fronto-temporal group probably inflated the mean score of the combined group of patients with removals involving the frontal lobes.

For all the groups combined, a positive correlation between risk-taking scores on the Visual Task Without Points and risk-taking scores on the Visual Task With Points (r = +0.45, P=O.OOl) indicated that subjects were consistent in the relative amount of first- card guesses made under the two motivational conditions. When Pearson product-moment correlations were done by group, however, it was found that only the NC, RT, and LT groups had risk-taking scores that were significantly correlated on the two tasks (NC: r = +0.53, P=O.O09, RT: r= +0.45, P=O.O5, LT: r= +0.44, P=O.O3).

No significant relationship was found between number of first-card guesses and site of cortical excision within the frontal lobe, nor between risk-taking scores and size of excision from either the frontal or temporal lobes. There was a positive correlation between the number of first-card guesses and the number of points won (r = -t- 0.30, P = 0.004) but there was no significant difference between groups on the mean number of points obtained, with

the NC group obtaining the highest mean number of points (408) and the LF group scoring the lowest (301).

Synthesizing ability

The synthesizing-ability score was the number of items eventually identified 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. For both risk-taking and synthesizing-ability scores, a response was accepted if subjects were able to describe adequately an item that they could not name. The ability to combine visual clues was correlated with Performance IQ (Visual Task Without Points: r = +0.26, P =0.03; Visual Task With Points: r = +0.30, P =O.Ol), but a one-way analysis of variance demonstrated no differences between groups with respect to Performance IQ. Synthesizing ability was also positively correlated with the number of points won (r = +0.69, P =O.OOl).

In the ability to synthesize fragments of visual information, the RT group differed significantly from the NC group on the Visual Task With Points, as shown by a one-way analysis of variance (F = 2.90, P ~0.05) and a Newman-Keuls post hoc comparison. Table 3

Table 3. Synthesizing ability: mean number of items correctly identified (maximum = 17)

Task Normal Right control temporal

Group Left Right Left Right-fronto-

temporal frontal frontal temporal

Visual Task Without Points Visual Task With Points

16.4 15.4

16.4 14.9* 15.6

15.8 15.2 15.1

15.0t 14.67

16.7

15.5

*Right temporal-lobe group differs from the normal control group (P~0.05). tWhen combined, the right frontal-lobe and left frontal-lobe groups differ from the normal control group

(P<O.O5).

366 LAURIE MILLER

shows that on both tasks the means for the RF and LF groups were nearly equal to the means obtained by the RT group but, probably because of the small number of subjects in each of the frontal-lobe groups, the scores of these groups did not differ significantly from the NC group on a post hoc test. When the LF and RF groups were combined, however, their mean synthesizing-ability score was indeed lower than that of the NC group on the Visual Task With Points (t = 3.25, P<O.Ol). There was no correlation between synthesizing ability and the size of cerebral excision from either the frontal or the temporal lobes.

Incorrect responses

Incorrect guesses were also examined in order to determine whether there were differences between groups in the ability to make use of the information available in the clues. Six independent judges were shown the cards that each subject had seen prior to making a wrong guess. These judges were then asked to decide whether the incorrect responses were possible target items, given the information available. A response was counted as a perceptual error

when at least four of the judges were unable to imagine that the item guessed could be constructed from the visual fragments.

The perceptual error scores were submitted to a square-root transformation (in order to satisfy the homogeneity-of-variance requirement for a one-way analysis of variance), and the F test was found to be significant for the Visual Task With Points (F=2.48, P~0.05). On both tasks, it was the RF and LF groups that made the most perceptual errors (see Table 4),

Table 4. Mean number of perceptual errors

Task Normal Right control temporal

Group Left Right Left Right fronto-

temporal frontal frontal temporal

Visual Task Without Points Visual Task With Points

1.65 2.70 2.48 2.73* 3.71* 1.83

0.74 0.80 0.84 1.91t 1.86t 1.17

*When combined, the right frontal-lobe and left frontal-lobe groups differ from the normal control group (PiO.05).

tWhen combined, the right frontal-lobe and left frontal-lobe groups differ from the normal control group (P<O.Ol).

but no between-group differences were found using a Newman-Keuls post hoc test at the 0.05 level of significance. When patients in the RF and LF groups were considered together, however, they did make significantly more perceptual errors than the NC group on both tasks (Visual Task without Points: t=2.46, P~0.05; Visual Task With Points: t=2.81, P<O.Ol). The extent of frontal-lobe excision from the medial, lateral or orbital surfaces was not significantly correlated with the number of perceptual errors made.

DISCUSSION

The first goal of this research was to provide a situation in which the impulsive behaviour occasionally exhibited by patients with frontal-lobe lesions might be elicited and measured objectively. The study demonstrated between-group differences only to a limited extent,

COGNITIVE RISK-TAKING AFTER FRONTAL OR TEMPORAL LOBECTOMY--I 361

possibly because the measure of impulsivity, guessing with only one clue available, was a

profitable strategy. (See MILLER and MILNER [22] for a report on tasks in which a high

number of first-card guesses was associated with a low points-score.) On the Visual Task Without Points, no differences were found between groups in the number of first-card guesses and, although on the Visual Task With Points a planned comparison revealed that a combined group of patients with frontal-lobe excisions averaged significantly more of these guesses than did the combined normal control and temporal-lobe groups, it was only the

patients with right fronto-temporal excisions that clearly showed a high score. Because the sets of clues used in the two tasks were apparently equal in difficulty (as

demonstrated by the number of items on each task eventually identified by the normal control group), the change in reinforcement condition, from no points being involved in the

first task to points being risked in the second, seems to have been responsible for both dampening the number of first-card guesses made by most groups, and for bringing out differences among groups. The right fronto-temporal group, which started out with a relatively high number of first-card guesses on the first visual task, also seems to have been somewhat less susceptible than other groups to the inhibiting effect of the increased risk in the

point-reinforcement condition, although there was no significant interaction between the

factors Group and Task. The second goal of the study was to assess the subjects’ ability to utilize fragmented visual

information in order to guess a whole object. Patients with right temporal-lobe excisions, as well as those with frontal-lobe excisions from either hemisphere, had some difficulty achieving the correct mental integration of the separated line fragments. Given the proven role of the right temporal neocortex in the perception and recognition of complex visual patterns [13, l&21, 23,24, 27, 281, it was expected that a right temporal lobectomy would

affect the ability to synthesize visual information. The difficulty displayed by patients with frontal-lobe lesions in identifying target items on the second task implies that the necessary perceptual operations differ from the ones involved in those visual tasks on which perceptual changes have been observed after posterior cortical damage but not after damage to the frontal lobes [S, 6,14,24,28,32,33]. Previous visuo-perceptual tasks have required subjects to make sense of a single image or figure but they have not asked subjects to imagine

segrated line-fragments forming a unified whole. The results of this experiment indicate that when comprehension of the relationship between separated components of a picture is necessary, patients with frontal-lobe lesions, as well as patients with right temporal-lobe lesions, have a deficit. It is not clear, however, why patients with right fronto-temporal excisions were not impaired on the measure of synthesizing ability taken from these visual tasks.

Some indication of the nature of the deficit in synthesizing abilities shown by patients with frontal-lobe excisions comes from the analysis of their incorrect responses. On the second visual task, these patients occasionally failed to utilize all of the information inherent in the material, thereby making significantly more perceptual errors than normal control subjects. On the Hooper Visual Organization Test [lo], patients with right frontal-lobe lesions have been noted to make similar errors [ 171; instead of imagining a juxtaposition of all the pieces of a cut-up drawing in order to identify the object represented, they tend to base their judgments on a single piece of the whole drawing. The relatively large number of perceptual errors made by the frontal-lobe groups on the present visual tasks support LURIA’S [IS] claim that patients with frontal-lobe damage seem unable to hold various fragments of information in mind as they manipulate and combine the separate components to form a cohesive whole.

368 LAURIE MILLER

Acknowledgements-This work is based on a thesis submitted by the author in September 1983 to McGill University in partial fulfillment of the requirements for the MSc. degree. The research was supported in part by a Max Bell (Open) Fellowship to theauthor and in part by grant MT 2624from the Medical Research Council ofCanada to Dr. Brenda Milner. I am grateful to Dr. Theodore Rasmussen, Dr. William Feindel, and their associates at the Montreal Neurological Hospital for the opportunity to study their patients, and to Dr. Brenda Milner for her supervision during the study and for her aid in the preparation of this paper.

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