Journal of Neurology, Neurosurgery, and Psychiatry 1985;48:1049-1053

Short report

Luria's frontal lobe syndrome: psychological andanatomical considerationsAGM CANAVAN,* I JANOTA,t PH SCHURRtFrom the Department ofExperimental Psychology, Oxford, * Department ofNeuropathology, t Institute ofPsychiatry, and the Neurosurgical Unit, The Maudesley Hospital, : London, UK

SUMMARY Luria has described a syndrome of disinhibited and impulsive behaviour, in which thepatient is unable to follow sequential instructions. This he attributes to localised frontal lobedamage. However, group studies of patients with focal lesions of the frontal lobes fail to revealsuch a syndrome. A patient is described who displayed a form of Luria's syndrome temporarily.Psychometric and post mortem evidence indicate that the syndrome arises only under conditionsof more global cerebral dysfunction.

Luria, Pribram and Homskayal described thefrontal-lobe syndrome thus: "The destruction of thefrontal lobes has relatively little effect on the courseof simple and well-consolidated motor stereotypes.Yet, the patient with frontal lobe destruction is oftenunable to fulfil instructions, is unable to inhibitimpulsive reactions or to hold back the tendencytowards fixed repetition of movement." In particu-lar, ". . . dissociation of verbal and motor reactionsis typicarl. These conclusions are based upon bed-side observations of the patient "Zav", a 43-year-old female office worker with a left frontal arach-noidal endothelioma (meningioma). This patientwas able to reproduce single movements with ease,but was unable to copy sequences of movements, orto produce sequences of movements to a singlecommand. She was also unable to repeat a series ofrhythmical beats made by the experimenter on apiece of wood with his pencil: the patienf s own tap-ping quickly deteriorated into a perseverative con-tinuous pattern. These behaviours were not due todefective appreciation of instructions; the patientwas able to repeat instructions verbally even whileproducing erroneous performances. In such circum-stances she was unable to say whether or not herperformance was correct.

Address for reprint requests: Dr AGM Canavan, Department ofExperimental Psychology, South Parks Road, Oxford OXI 3UD,UK.

Received 29 August 1984 and in revised form 5 February 1985.Accepted 9 February 1985.

This syndrome has only rarely been reported indetail. Another case is that of IS, a 69-year-oldhousewife suffering from Hodgkin's disease, withmetastasis to the left frontal lobe.2 This patient wasexamined four weeks after subtotal removal of theinfiltrating tumour. As with the first patient she wasable to follow simple commands, but unable to per-form serial tasks. In a figure-drawing exercise shedisplayed gross perseveration: at one point she drewthe letter "A" in response to almost any command.Unlike the first patient she indicated that she knewshe was making an error. Nevertheless this did notaffect her performance.Group studies of patients with frontal lobe lesions

have failed to reveal a syndrome as consistent as thatdescribed by Luria. Anecdotal evidence obtainedduring maze-learning supports Luria's claim,3 butmore recent work employing the same task found nosuch evidence.4 A task designed specifically toexamine the relation between verbal performanceand motor performance failed to find the predicteddissociation.5 Thus it has been concluded that such adissociation is not a general feature of the perfor-mances of patients with frontal lobe lesions.4

Nonetheless, the existence of even a small numberof patients exhibiting this syndrome is of theoreticalinterest. The precise localisation of the pathologyunderlying the syndrome would be of value. Thepatient described by Luria et al was operated uponwithin days of the examination, but died of heartfailure about 24 hours after the operation. Histo-logical examination revealed relatively widespread

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pathology of the left hemisphere, as well as limitedpathology of the right. The anterior edge of thetumour remnant was 4-5 cm from the frontal pole,the diameter of the defect being 7 cm in theanterior-posterior, 4 cm in the transverse and2 8 cm in the dorsoventral direction. The wholehemisphere was markedly oedematous, the cingu-late gyrus and the corpus callosum were distorted,and the head of the caudate nucleus was compres-sed. In addition both hippocampal gyri were pushedmedially, cut by a deep furrow with traces of pres-sure at the edge of the tentorium cerebelli, and theposterior horn of the right lateral ventricle wasdilated. Despite these massive lesions Luria specu-lated ". . . that the more generalised brain damagebrings out in relief . . . the essence of a disturbanceproduced by a local lesion",' although he did notspecify any particular location within frontal cortex.The case IS did not shed any further light upon thisissue, since the results of a post mortem examinationhave not yet been reported. Other cases describedby Luria,6-8 are similarly lacking in detailed pathol-ogy, the usual description amounting to little morethan the statement "A patient with a massive frontallobe tumour". A recent case of our own, JH, hasbeen reported briefly elsewhere,9 and since postmortem evidence is now available a fuller descrip-tion is warranted.

Case historyJH was a 64-year-old retired dance teacher, with a 6month history of numbness of the left leg below the knee.The numbness had first been noticed after she had beenfound unconscious on the floor. She had been sick but notincontinent. Previous to this she had been witnessed tosuffer an absence attack, though without shaking or falling.The numbness progressed and she was said to becomeforgetful and irritable". Upon admission she was orien-

tated in time and place, but unable to remember verbalmaterial over short periods. There was papilloedema inboth eyes and anosmia on the left. There was slight weak-ness of the left leg with impairment of the joint positionsense of the left foot. A CT scan and bilateral carotidangiography revealed a very large posterior frontal (mid-line) falx meningioma invading the superior sagittal sinus.The tumour, measuring 7 cm in diameter, was subse-quently removed in its entirety. Psychological investiga-tions commenced on the thirteenth postoperative day andcontinued for a month, when the patient was discharged.She was subsequently seen as an outpatient several times,until the point sixteen months after surgery when she suf-fered a myocardial infarction and died.

Description of the syndromeOn the thirteenth postoperative day JH displayed all of thesymptoms characteristic of the frontal lobe syndromedescribed above: there was marked motor perseverationboth in spontaneous behaviour (for instance, she displayeda tendency to tap or rub parts of her body continuously),

Canavan, Janota, Schurrand also while copying drawings (for instance, after com-pleting a straight line or a square she would then retraceeach line vigorously until it was about half a centimetrethick). When asked to copy a continuous but castellatedline she would produce several lines of completed squares.This motor perseveration occurred relatively indepen-dently of verbal control. If asked to stop during the courseof tapping or drawing, she would say "yes" but continueregardless. If she herself said I will stop now" thebehaviour also continued unchecked. However, if she wasasked to start a different activity (for example placing herhands by her side) she was able to do so and thereby termi-nate the previous activity. At this time, when asked to fill inthe numbers on an empty clock-face, she would draw asmany numbers as could be fitted on the face, starting with a1" in the appropriate place and counting upwards until

returning to the 1" position. This often resulted in four-teen or fifteen numbers, although she was quite clear uponquestioning that there could not be a fourteen o'clock" or"fifteen o'clock" time.Apart from these informal tests, JH also underwent

standardised psychometric examination. These procedureshave not previously been employed with patients display-ing the frontal lobe syndrome.' 2 68 On the thirteenthpostoperative day JH was found to have a WAIS verbal IQof 63, and a performance IQ of 61'1 (see table for indi-vidual subtest scores). Since JH could be presumed to havebeen of average premorbid intelligence, this is evidence ofgeneralised deterioration, which is not normally seen fol-lowing circumscribed frontal lobe lesioning.34 A short formof the Minnesota Dysphasia Battery" revealed some minorverbal deficits. JH did well at tests of reading and spelling,but displayed difficulty in naming pictures (although only2/20 errors) and in identifying items serially (2/6 errors).This deficit was not purely expressive dysphasia, since apicture vocabulary test'2 which requires only pointing as aresponse yielded an IQ of 56, which is close to thoseobtained from the WAIS. Verbal memory was alsoimpaired. Immediate recall of two stories'3 was 3/23 and0/23 items respectively. She also did poorly when asked toremember ten series each of ten words.'4 Her average wasone item per list compared to the average for the normalpopulation, which is about 6- 5 items per list. Delayed recallof nonverbal material'5 was also impaired. Thus it wouldappear that psychometric investigation of the frontal lobesyndrome described by Luria reveals not so much a patternof specific impairments but rather a complex generalisedintellectual disruption.

Table Individual WAIS age-scaled subtest scores at thetime of initial assessment and one month later

Subtest First occasion Second occasion

Comprehension 3 10Similarities 2 10Vocabulary 3 10Digit span 6 8Block design 0 10Object assembly 5 11

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Luria's frontal lobe syndrome: psychological and anatomical considerations

Course of the syndromeThe motor perseveration observed on the thirteenth post-operative day proved to be a relatively transient phenome-non. By the seventeenth postoperative day JH was showingsigns of improvement in her ability to copy drawings, andon the eighteenth postoperative day and subsequently shewas able to perform such tasks without difficulty.Psychometric assessment was repeated one month after theinitial examination, and this time JH scored mainly in thenormal range (for example verbal IQ 94, performance IQ107-see table for individual subtest scores). It was stillpossible to detect perseveration on a card sorting test,'6 asis common in patients with circumscribed frontal lobelesions, but the gross perseveration characteristic of thesyndrome described by Luria had by this time completelydisappeared. Fluency tests3 1" also elicited impairments, aswould be expected of a patient with bilateral frontal lobedamage. In short, the syndrome described by Luriaappeared only in the context of widespread intellectual

dysfunction in the immediate postoperative period. Withinweeks this syndrome had disappeared, leaving in its wakeonly the more subtle deficits known to be associated withfrontal lobe damage. None of the cases described by Luriaand his colleagues have been administered standardisedtests of the kind described here, and thus it might be thatwidespread intellectual dysfunction is a prerequisite for thesyndrome to appear. In the present case it must beassumed that the immediate postoperative syndrome arosethrough the temporary effects of oedema or disrupted cir-culation.

Postmortem evidencePostmortem examination revealed the extent of braindamage responsible for the more permanent but more sub-tle deficits. This evidence also shed light upon the extent ofbrain damage necessary to produce the syndromedescribed by Luria.The fresh brain weighed 1060 g. When fixed and after

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Fig Nine coronal slices through the cerebral hemispheres numbered A to 1 from in front. Arrows in G andH indicate thecentral fissures (ofRolando). Arrowhead in E points to the scar in the right thalamus. Note a small hole in the left globuspallidus in D. The loss ofcingulate cortex is seen on the left in C and on the right in D. The anterior part ofthe corpuscallosum, but not the genu, is abnormally thin. The extent ofthe tumour was from B to E.

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1052slicing, it weighed 996 g. There was a ragged defect 5 cmlong and about 4-5 cm wide in the mid frontal parasagittalregion, roughly corresponding to the site of the mening-ioma that had been removed previously. The borders ofthe defect included grey fibrous meningeal tissue andorange-yellow old iron pigment. Inspection of the undersurface of the brain showed patchy atheroma withcalcification and narrowing of the lumen of the largerarteries. There was bilateral uncinate grooving some 3 mmfrom the medial border, a little deeper on the left wherethere was also some grooving in the parahippocampalgyrus. Coronal slicing of the cerebral hemispheres (fig)showed a patchy loss of cortex and scarring in the whitematter in the defect that was seen from the outside.Anteriorly, scars in the convexities, about 1-5 cm from themidline, extended to within 2 cm of the frontal poles. Thewhite matter between the outer surface of the top of thehemispheres and the ventricles felt soft and looked lesswhite than normal. This abnormality extended posteriorlyto the central fissure, more so on the right. There was aseparate small cavitated cortical scar in the posterior upperborder of the right frontal convexity. The cingulate gyriwere preserved except for some cortical loss deep to thedefect and softening of the white matter on both sides atthat level. The corpus callosum was thinner than normalfor some 3 cm posterior to the genu. The lateral ventricleswere very much dilated with a stretch of white matterseparating the caudate nuclei from the corpus callosum.There were two other old scars: one cavitated about 4 mmin diameter in the medial border of the left globus pallidusat the level of the genu of the internal capsule, and onenarrow grey streak 3 mm long in the anterior part of theright lateral thalamus deep to the lateral ventricle. Therewere no lesions in the brain stem or cerebellum or spinalcord.

Discussion

At necropsy there was widespread cortical and sub-cortical pathology. It is likely that the preoperativemotor and sensory clinical abnormalities wererelated to the old lesions in the right convexity orthalamus. The lesion in the left pallidum may nothave given rise to any symptoms or signs. It is a littleanterior to the old target area for stereotactic lesionsin Parkinsonism. The lesions in the brain in the bedof the tumour may well have been affected bysurgery; these and the cortical and white matterabnormalities more anterior and posterior probablyrelate to a disturbance of the circulation through thesuperior saggital sinus caused by the tumour. Theanterior cerebral arteries appeared normal andthere was no evidence to suggest the presence ofarterial infarcts. The location and extent of theabnormalities match the dearth of neurologicalsigns; they are consistent with a relatively good levelof intellectual performance before, and later afterthe operation. The reference to forgetfulness sometime before her admission, and to poor short-termmemory on admission, may hold implications for a

Canavan, Janota, Schurr

disturbance of the limbic circuit at the level of theabnormalities in the cingulate gyri, in the absence ofany other visible lesions. Histological examinationhas not been carried out because it seemed veryunlikely that it could help with either the anatomy orthe pathogenesis of the obvious abnormalities.The widespread frontal lesions described here can

account for the long term subtle psychological dis-turbances seen in this patient. However, even thegross damage noted above was not sufficient to sus-tain the "frontal lobe syndrome" described byLuria. This casts some doubt upon Luria's assertionthat the syndrome reflects focal frontal dysfunction,especially since group studies of patients with cir-cumscribed frontal lobe lesions fail to reveal such asyndrome. Nevertheless when the syndrome isreported it is associated with frontal lesions and notas a rule with occipital, temporal or indeed globallydementing conditions. The evidence presented herewould suggest that the syndrome is not produced bya frontal lesion alone, but by a frontal lesion in asetting of more global cerebral dysfunction fromdisplacement, distortion or oedema.

References

Luria AR, Pribram KH, Homskaya ED. An experimen-tal analysis of the behavioural disturbance producedby a left frontal arachnoidal endotheliona (mening-ioma). Neurophysiologia 1964;2: 257-80.

2 Konow A, Pribram KH. Error recognition and utilisa-tion produced by injury to the frontal cortex in man.Neuropsychologia 1970;8:489-91.

3 Milner B. Some effects of frontal lobectomy in man. In:Warren JM, Akert K, eds. The Frontal Granular Cor-tex and Behaviour. New York: McGraw Hill, 1964.

4Canavan AGM. Stylus-maze performance in patientswith frontal-lobe lesions: effects of signal valency andrelationship to verbal and spatial abilities. Neuro-psychologia 1983;21: 375-82.

Drewe EA. An experimental investigation of Luria'stheory on the effects of frontal lobe lesions in man.Neuropsychologia 1975; 13:421-9.

6 Luria AR, Homskaya ED. Disturbances in the regula-tive role of speech with frontal lobe lesions. In: War-ren JM, Akert K, eds. The Frontal Granular Cortexand Behaviour. New York: McGraw Hill, 1964.

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8 Luria AR. The Working Brain. Middlesex: PenguinBooks, 1973.

9Canavan AGM. Single case methodology in neuro-psychology. In: Lindsay SJE, Powell GE, eds. AHandbook ofClinical Psychology. London: Gower. Inpress.

'0 Wechsler D. Wechsler Adult Intelligence Scale. Manual.New York: Psychological Corporation, 1955.

" Powell GE, Bailey S, Clark E. A very shortened versionof the Minnesota Aphasia Test. Br J Soc Clin Psychol1980; 19:189-94.

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Luria's frontal lobe syndrome: psychological and anatomical considerations12 Dunn LM. Peabody Picture Vocabulary Test. Minnesota:

American Guidance Service, 1959.II Wechsler D, Stone CP. Wechsler Memory Scale. Manual.

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16 Nelson HE. A modified card sorting test sensitive tofrontal lobe defects. Cortex 1976;12:313-24.

7 Jones-Gotman M, Milner B. Design fluency: the inven-tion of nonsense drawings after focal cortical lesions.Neuropsychologia 1977; 15:653-74.

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