Neuropsychologia. 1975, Vol. 13, pp. 421 to 429. Pergamon Press. Printed in England.

AN EXPERIMENTAL INVESTIGATION OF LURIA’S THEORY ON THE EFFECTS OF FRONTAL LOBE

LESIONS IN MAN

E. A. DREWE

Institute of Psychiatry, De Crespigny Park, London SE5 SAF, England

(Received 30 December 1974)

Abstract-Tasks on which Luria has predicted patients with lesions of the frontal lobes would be impaired were given to 48 patients with unilateral localised lesions. Deficits were found, although the nature of impairments and their relationship to specific locus of lesion were not as predicted. In patients with frontal lobe damage, relatively unimpaired verbal responses were found in association with defective motor responses on one task only. The inability to utilise overt verbalisation to regulate motor performance was likewise found to be not as general as Luria has hypothesised. The deficits are discussed in relation to known effects of frontal lesions in man and non-human primates.

INTRODUCTION

LURIA has postulated that, after damage to the prefrontal cortex, patients are unable to form “action plans” and cannot match response outcome with the original intention formulated by such plans [l-5]. He considers that in young children “plans” are visually or kinaesthetically controlled whereas in older children and “normal” adults verbal mediation is of primary importance. Luria claims that a disorder of the regulation of voluntary movements by language is one of the earliest manifestations of a frontal lobe lesion in humans and that this frequently remains as the last symptom when other disturbances have cleared [3].

As evidence for the theory, Luria observes that patients with frontal lesions perform poorly on tasks which necessitate the organisation of a series of actions in response to verbal directives and which may to varying extents conflict with kinaesthetic or visual cues or the motor impellant function of speech. Although able to comprehend instructions, they are unable to make use of them to regulate behaviour. Similarly, they are able to produce correct verbal responses on the same tasks but these do not aid organisation of motor responses of the hand. In contrast, patients with lesions in other cortical areas are able to carry out such tasks successfully provided they have adequate comprehension and motor control. However, even if such impairments are evident in patients with non-frontal lesions, their own explicit verbal responses are able to regulate and improve motor performance [3].

Luria claims that the deficits described are primarily associated with lesions of the left frontal convexity [6], although some patients with right frontal damage have been shown to be impaired [l, 31.

Luria’s descriptions of deficits found after lesions of the frontal lobes are based mainly on the performance of patients on three types of task. These are (i) tasks involving “press” and “don’t press” responses, (ii) tasks involving responses with the left and right hands, and

421

422 E. A. DREWE

(iii) conditional tasks in which the directive function of the stimuli conflict with the meaning given to them by verbal instructions (e.g. directed to tap once on hearing two taps and twice on hearing one tap). Explicit details of procedures and patients are not however described. The present experiments were undertaken to systematically investigate the performance of groups of patients with lateralised frontal or non-frontal cortical lesions on such tasks to ascertain whether or not deficits of the type described by Luria could be elicited. The importance of specific locus and laterality of lesions within the frontal area and the effects of overt verbalisation were also investigated.

METHODS Patients

Forty-eight patients (l’s) were tested. Each had a damage in one of 4 mutually exclusive areas of the cortex: left frontal (LF), right frontal (RF), left “non-frontal” (LNF) and right “non-frontal” (RNF). There were 12 patients in each group. Site of lesion was confirmed by surgeon’s written operation reports in all but one case (a RNF diagnosed by AEG). Patients with frontal lesions were also classified according to locus of lesion within the frontal area. Eight LF and 10 RF had medial lesions, 7 LF and 6 RF had dorslateral lesions and 4 LF and 7 RF had orbital lesions. These subgroupings were not mutually exclusive. In the group of patients with non-frontal lesions 9 LNF and 6 RNF had exclusively temporal lobe damage, 2 LNF and 1 RNF temporal and parietal damage, 1 LNF and 4 RNF exclusively parietal injury and 1 RNF an occipital lesion.

In order to determine the effect of motor impairment on performance, the presence or absence of motor deficits was evaluated for each patient. Such deficit was concluded to be present if any indication of paralysis or poor motor control was recorded in the case notes by a neurosurgeon or neurologist. Two patients with frontal lesions (Fs) and 3 patients with non-frontal lesions (NFs) had motor deficits.

There were no significant differences between lesion groups (by analyses of variance or Fisher Exact Probability Tests) in terms of age of patients, chronicity of lesion, as defined by time in years since the first indications of brain damage, or distribution of types of lesions (Table 1). Intelligence was measured on a short WAIS [7]. There were no group differences-on the verbal factor although-patients with right hemi- sphere damage achieved lower scores on the performance factor than those with left injury (P < O.Ol), the difference between RF and LF groups being less than that between LNFs and RNFs (locus x laterality interaction P < 0.01). Further details of patients may be found elsewhere 181.

Apparatus The apparatus, as seen by the patient, consisted of a 18 cm x 30 cm upright on which were displayed

4 small and 2 large lights. These were coloured and arranged as indicated in Fig. 1. Directly under each pair of small lights and projecting forward was a morse key, 18 cm long with a head 3 cm in dia. The onset and offset of each light could be controlled by the experimenter (E). In addition, P could switch off a large light by pressing one of the morse keys. The “correct” key was determined on each trial by E.

All lights and switches were connected via relays to a 2 channel tape recorder with a built-in tone generator. Onset of a large light initiated a tone signal on one channel of the tape. Depression of the “wrong” key by P (i.e. the one other than that designated as correct by E) initiated a signal on the second channel. Light offset, by depression of the correct key, or by E, terminated signals on both channels. A recording could therefore be made of the latency and correctness of responses. The tape was analysed on a LTNC 8 computer.

ORed light @Blue light

Fro. 1. Display as seen by patient.

INVESTIGATION OF LURIA’S THEORY ON THE EFFECTS OF FRONTAL LORE LESIONS IN MAN

Table 1. Patient variables

423

Lesion GIZOUD

a) Nature of Lesion LF RF INF RNF

I

II

III

Space-Occupying Lesion

Intrinsic tumour e.g. glioma, astrocytoma

Extrinsic tumour e.g. meningioma

Abscesses

Lobectomy for epilepsy

(of multiple aetiology e.g. mesial temporal sclerosis, atrophy, small tumour)

Other.

CVA

Penetrating head injury

Localised atrophy

Localised epileptic focus of unknown aetiology

Unilateral leucotomy

b) Chronicity of Lesion (in years)

si Sd

awe

c) Age

F

Sd

Range

d) Intelligence

Verbal Factor IQ 'ji

Sd.

Range

Performance Factor IQ

z sa

4 3 6

3 3 1

20 0 8 6 7 - - -

0 0

1 1

0 1

0 0

-IO

2 2 - -

3.28 3.47

2.59 3.97

4

3

22 7 -

2 2

_I!

3 -

2

3 -

3.80 4.59

5.74 5.89 .02-8 .02-10 .04-17 .06-17

38.5 35.9 30.6 37.5

12.5 13.5 14.5 14.1

20-60 17-60 17-58 20-55

102.9 106.9 94.6 106.6

17.0 18.8 17.1 16.9

76-132 74-139 68-128 79-124

96.0 92.1 119.2 78.1

14.4 14.1 16.1 23.2

73-126 67-110 90-146 43-113

424 E. A. DREWE

Procedure P was seated in front of the apparatus. The relationship between lights and switches was then explained

and demonstrated. Following this, 20 simple reaction times with each hand were given in order to accustom P to the apparatus and to emphasise speed of response.

Four tasks were then given. 1. Go--no go (GNG). P placed his preferred hand on a key. He was instructed to press this as quickly as

possible to large red light onset but to refrain from pressing when the large blue light came on. ITI 1-3 sec. Thirty red and 30 blue lights were presented according to a Gellermann schedule. Pressing the key extin- guished the red light but not the blue. The blue light, or the red light if P failed to respond, was switched off by E after 10 sec. In trials 2140, P was instructed to make a verbal response in addition to the “motor” one. Thus, he was to say “yes” and push the key to the red light and to say “no” and refrain from pushing the key to the blue.

2. Go right-go left (R-L). P placed one hand on each key. He was instructed to press the right hand key to large red light onset and to press the left hand key to large blue light onset. Large red and blue lights were each presented 30 times, randomised according to a Gellermann schedule. ITI 3-5 sec. Depression of the correct key extinguished the light. After an incorrect response E switched off the light after 5 sec. An additional verbal response was requested in trials 2140. P was instructed to say “right” to red light onset as well as pressing the right hand key and to say “left” to blue light onset as well as pressing the left hand key.

3a. Compatible conditional discrimination (CCD). In this task the colour of the stimulus cue is the same as that of the response cue, thus providing a control for 3b. On each of 60 trials, 3 lights were illuminated: one small blue, one small red on the opposite side, and a large light. The colour of the large light and the relative position of the small lights were determined by two superimposed Gellermann schedules. P rested one hand on each key and was instructed to press the key under the little red light, regardless of its side of appearance, when the large red central light was illuminated, and to press the key under the little blue light to large blue light onset. Correct key depression extinguished the central light. All lights remaining on were switched off by E 5 set after a response. IT1 3-5 sec. In trials 2140 P was instructed to say “blue” in addition to pressing the key under the small blue light and to say “red” in addition to pressing under the small red light, to large blue and large red light onset respectively.

3 b. Incompatible conditionaI discrimination (ICD). In this task the stimulus and response cues are different in colour. The procedure was similar to that described for CCD except that P was instructed to press the key under the &all blue light to large red light onset and to press the key under the small red light’ to large blue light onset. In trials 2140 P was instructed to say “blue ” in the former case and “red” in the latter, i.e. to verbalise the colour of the small light beneath which the response was to be made.

In each task, speed of response was emphasised and P was asked to make only one response on each trial. Full details of instructions and orocedure are described elsewhere 181. GNG was given first, and on a different day to the other three tasks. RfL, CCD and ICD were performedin the same s&ion in an order which was systematically varied across patients. All 6 possible orders were given, 2 patients in each lesion group per- forming the tasks in each order.

As a measure of verbal comprehension part 5 of the Token Test [9] was also given to each patient.

RESULTS

Statistical analyses are by Chisquare tests, Mann-Whitney tests or analyses of variance unless otherwise stated. Generally only “significant” results (I’ < 0.05 on a two tailed test or P < O-025 on a one tailed test) are given. Full details of findings are given elsewhere [S].

Motor responses The numbers of motor (hand) response errors made by each lesion group are given in

Table 2. GNG. False positive (FP) responses (pressing to the blue light) were made by more

Fs than NFs (P < 0.01). Of Ps making such errors, Fs made more than NFs, both in the total 60 trials (P < O-05) and in trials with only motor responses (P < 0.05). In order to assess trend over trials, a comparison of number of FPs in trials I-30 and 31-60 was made. NFs improved significantly over these blocks (Wilcoxon Test, P < O-05) whereas Fs did not. Jn no case did LFs differ from RFs. Only 5 Ps, 1 RF, 1 LNF and 3 RNFs, made false negative (FN) errors (not responding to the red light). Within this group there was a perfect positive rank order correlation between number of FN and number of FP errors made.

INVESTIGATION OF LURIA’S THEORY ON THE EFFECTS OF FRONTAL LOBE LESIONS IN MAN 425

Table 2. Errors made on tasks

No. Ps z No. Median Range making error8 errors errors made

a (False Positives only)

LF 10 3.3 2 O-10

RF 11 2.4 2 0- 5

ml? 7 2.2 1 o-11

FINF 7 1.4 1 o- 5

LF 11 2*9 2 0- 9

RF 0 2.2 2 0- 7

LNF 8 1.7 1 0- 5

9 1.4 1 0- 3

Ill? 11 11.8

RF 11 11.8

LNF 9 1.8

RNF 10 8.0

gJ

IJ?

RF

LNF

?tNF

11 19.6 25 0-36

9 11.7 11 o-32

9 2.4 2 0- 6

9 9.4 4 o-24

O-30

O-26

0- 6

o-31

R-L. There is no significant difference between groups in number of Ps who made errors, number of errors made or trend over trials. Order of task performance did not affect results. CCD. Fs made more errors than NFs, both in the total 60 trials (P < OeOl), and in the

40 trials requiring only a motor response (P < 0.01). There was no significant difference

426 E. A. DREWE

between RFs and LFs in error rate. The number of errors made did not differ across the 6 task orders, nor was there any trend across blocks of trials.

ZCD. Fs made more errors than NFs in the total 60 trials (P < O*Ol) and trials requiring only a motor response (P < 0.05). LFs made more errors than NFs (P < O*Ol). Perform- ance did not vary across the 6 orders nor was there a trend over trials.

Ps overall made more errors on TCD than on CCD tasks (P = 0.02) although there was a locus x laterality interaction in this respect (P = 0.04). Taking each lesion group separ- ately, only LFs performed more poorly on ICD than on CCD (Wilcoxon, P < 0.05). A similar tendency was not significant in either LNFs or RNFs, and in RFs the trend was in the opposite direction.

Errors made on R-L, CCD and ICD intercorrelate together in Fs, but none are asso- ciated with GNG performance (Table 3). In NFs ICD performance correlates with that

of all other tasks.

Table 3. Intercorrelations (11~) between tasks

Frontals

GNG R-L

R-L 033

CCD .oo .41*

ICD .11 .43*

CCD

.72-

Nor&Frontals

GNG R-L CCD

R-L 933

CCD .30 .Ol

ICD l 49* .47* .58*

* p.c.05

-)Hc p<.Ol

Verbal responses There is no difference between groups in number of verbal response errors made on

GNG or R-L tasks. Fs made more verbal errors than NFs on CCD (P < 0.01) and on ICD

INVESTIGATION OF LURIA’S THEORY ON THE EFFECTS OF FROh-rAL LOBE LESIONS IN MAN 427

(P < 0.05). On ICD, however, LFs made more verbal errors than each of the other groups (P < 0.05 in each case). In no task did the ratio of correct motor responses in trials 21-40 to correct verbal responses differ between Fs and NFs.

As a measure of compatibility of motor and verbal responses, the number of times in trials 21-40 that the motor response failed to correspond with the verbal one, regardless of which was correct, was calculated. Groups did not differ on this measure on R-L or GNG tasks. On ICD, LFs made more such incompatible responses than either RFs or LCs (P < 0.002 in each case). On CCD, comparing just those patients who made incompatible responses, Fs made more than NFs (P < 0.05).

The effect of verbal responses on motor performance was assessed by comparing motor response errors in trials 21-40 with the number expected from averaging those incurred on trials l-20 and 41-60. Observed and expected values did not differ on GNG. On R-L, the number of motor errors made on trials with verbal responses was less than that expected from the other trials (P < 0.01). This was found, however, for all lesion groups. On CCD and ICD there is a difference between Fs and NFs in the distribution of errors over trials with and trials without verbal responses (P < 0.05 in each case). In both tasks NFs made more errors on trials requiring only motor responses than on verbal trials. Fs, on the other hand, made a similar number of errors on each set of trials on ICD, and made more errors on verbal trials than on trials requiring only a motor response on CCD.

Token Test scores are significantly associated with error rate on all 4 tasks in Fs (GNG rs = 0.46, P < 0.05; R-L rs = 0.72, P < 0.01; CCD r, = O-49, P < 0.05; ICD Y, = 0.44, P < 0.01). There were no associations in NFs.

In the total P group, age and IQ are not correlated with performance on any task. Type of lesion did not affect performance on any task in either Fs or NFs (by Kruskal-Wallis analyses), nor was there a difference in any group between Ps with and Ps without motor deficits.

Locus of lesion within the frontal lobes was not associated with poor performance on any task in Fs as a group. In LFs, Ps with medial damage were worse than NFs on ICD (P < 0.01). In RFs, Ps with frontal lesions excluding the dorsolateral area were worse than NFs on CCD and ICD (P < 0.05 in each case), those with “non-medial” frontal lesions worse than NFs on R-L (P < 0.05) and those with “non-orbital” frontal lesions worse than NFs on GNG (P < 0.05).

DlSCUSSION

Patients with lesions of the frontal lobes were found to be impaired in the tasks given in the present experiment. The increase in false positives but not false negatives found on the go-no go task is not consistent with observations reported by Luria. Similarly, the poor CCD performance suggests that the reason for impairment on ICD was not as hypo- thesised by Luria. R-L performance was correlated to that of ICD and CCD in patients with frontal lesions. However only patients with right “non-medial” frontal lesions were significantly worse than the control group on this task. There is no evidence therefore that the type of deficit found on the tasks is as Luria has suggested.

A disruption of motor performance by verbalisation and inconsistency of motor and verbal responses was found only on CCD and ICD. On only GNG was intact verbal performance found in the presence of motor impairment. The dissociation of verbal and motor behaviour can, therefore, be demonstrated in only specific instances. It appears,

428 E. A. DREWE

from the present experiment, not to be an important general feature of performance of patients with frontal lesions.

The impairments found on the tasks are however, similar to the deficits elicited on learn- ing tasks in non-human primates with bilateral frontal lobe lesions. The failure to inhibit approach responses and the increasing error rate over time on go-no go tasks in monkeys has been well documented [!@-121. “Non-spatial” conditional discrimination deficits in non-human primates with frontal lesions have also been indicated [13, 141 and these may be dissociable in terms of critical lesion area from impairments on go-no go tasks [14]. In the present experiment, GNG performance did not correlate with that of CCD and ICD in patients with frontal lesions. The critical lesion area also differed for these two types of task. The nature of the deficit on go-no go and non-spatial conditional tasks may thus differ. Although R-L performance correlated with that on CCD and ICD, only patients with non-medial lesions of the right frontal lobe were impaired. This may reflect a com- mon factor in tasks which involve a choice between two approach responses. It, at the same time, emphasises the dissociation of performance on “spatial” and “non-spatial” tasks. This susceptibility of learning on spatial tasks to more than one type of deficit has also been found in non-human primates [15].

The tasks used in the present experiment did not involve learning. In non-human pri- mates, disturbance of frontal lobe function may impair performance under certain con- ditions as well as learning [12, 161. Deficits have also been described in man on learning versions of some of the tasks given in the present experiment [S, 171. However, in man, intercorrelations between the learning tasks differed from those between the “perform- ance” ones, and the critical lesion area was also found not be be identical [8]. Thus al- though the “performance” impairments may appear similar to those on the learning tasks, the nature of the deficits may not in fact be the same.

Deficits on “spatial” learning tasks have been found to be associated with unilateral right frontal lesions in man and to be dissociable from performance on “non-spatial” learning tasks [ 181. The present results extend this finding to non-learning tasks. However, as has been found on a go-no go learning task and on the Wisconsin Card Sorting Test performance [ 17, 191, deficits on non-spatial performance tasks are found after unilateral lesions of either laterality. Further experimental work is necessary to ascertain whether deficts on the non-spatial tasks given in the present experiment are non-unitary.

No non-brain damaged subjects were tested in the present study. The performance of the NF group was not related to the presence of motor or verbal comprehension deficits and the non-learning nature of the tasks minimises the effect of memory difficulties. It is possible however, that the NFs may be impaired compared to non-brain damaged subjects for other reasons. If they are, then this might mask the deficits of patients with frontal lesions. It is clear that patients with frontal lobe lesions do have difficulty with the tasks given in the present study. Their exact nature and similarity to those found in non-human primates must be determined by future research.

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BRAZIER (Editor). 3rd Macv Conference. Instit. Mental Health, Bethesda, Marvland. 1960. 2. LURIA, A: R. and HOMSK~YA, E. D. Disturbances in the regolative role of s$eech.with frontal lobe

lesions. In The Frontal Gramdar Cortex and Behavior, J. M. WARREN and K. AKERT (Editors). McGraw- Hill, New York, 1964.

3. LURIA, A. R. Higher Cortical Functions in Man. Tavistock, London, 1966. 4. Luara, A. R. Human Brain and Psychological Processes. Harper & Row, New York, 1966.

INVESTIGATION OF LomA’S THEORY ON THE EFFECTS OF FRONTAL LOBE LESIONS IN MAN 429

5. LURIA, A. R. The regulative function of speech in its development and dissolution. In Research in Verbal Behaviour and Some Neuropsychological Implications, K. SALZINGER and S. SALZINGER (Editors). Academic Press, New York, 1967.

6. LIJRIA. A. R. Frontal lobe syndromes. In Handbook of Clinical Neurology, P. J. VINKEN and G. W. BRUYN (Editors). Vol. 2, North Holland, Amsterdam, 1969.

7. MAXWELL, A, E. Obtaining factor scores on the Wechsler Adult Intelligence Scale. J. ment. Sci. 106, 1060-1062, 1960.

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11. BRUTKOWSKI, S. Prefrontal cortex and drive inhibition. In The Frontal Granular Cortex and Behavior, J. M. WARREN and K. AKERT (Editors). McGraw-Hill, New York, 1964.

12. ROSVOLD, H. E. and MISHKIN, M. Non sensory effects of frontal lesions on discrimination learning and performance. In Brain Mechanisms andLearning, J. F. DELAFRESNAYE (Editor). Blackwell, Oxford, 1961.

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15. MISHKIN, M. Perseveration of central sets after frontal lesions in monkeys. In The Frontal Granular Cortex and Behavior, J. M. WARREN and K. AKERT (Editors). McGraw-Hill, New York, 1964.

16. STAMM, J. S. Electrical stimulation of monkey’s prefrontal cortex during delayed-response performance. .I. camp. Physiol. Psychol. 67, 535-546, 1969.

17. DREWE, E. A. Go-no go learning after frontal lobe lesions in humans. Cortex, to be published, 1975. 18. MILNER, B. Interhemispheric differences in the localisation of psychological processes in man. Br. med.

Bull. 27,272-277, 1971. 19. DREWE, E. A. The effect of type and area of brain lesion on Wisconsin Card Sorting Test performance.

Cortex 10, 159-170, 1974.

011 disclxtf cfs deficits dans leurs relations avec les donnFes slur les fffeta des lesions frontalrs chcz l’homme et les primates non

bumains.

Deutschsprachige %usar,menfassung:

48 Patienten mit einseitig lokalisierter LIsionen vrurder, Aufgaben gegeben, “on denen LURIA vorzusgesagt hat, da8 Patienten nit L&ionen der E’rontallappen irjhrer Leistung beeintrlchtigt seien. Es ururde1-i zwar i.;inderungen gefunden, wenn such die tit der StBrungen und ihre Bindunz an den spezifischen LXsionsort nic.1 ‘t wie vorhergesagt beschaffen waren. Bei Fatlenten nit Schsdigung eines Frontallappens wurden relativ stFrungsfreie sprachliche Xmiderungen in Verbindung mit gestiirter motorischer Reaktion nur bei einer Aufgabe gefunden. Desgleichen wurdc herausgefunden, da8 das UW3iTCgen, offensichtliche WbalisierungsfBhigkeit zur Steuerung der motorischen Leistung zu gebrauchen nicht unbedingt (wie in LURIAs Hypothese) verallgemelnert werden darf. Die Leistungsminderungen werden in Verbindung mit bekannten Auswirkungen frontaler L;isionen bein i.:enschen und bei nicht-menschlichen R-inaten diskutiert.