A re-appraisal of a case of persistent global amnesia following right temporal lobectomy: A clinico-pathological study

Aeurrp,yrimlnym, VoL311, No . t, pp .43i-450 1992

(1714 3932,92 5500 F 000 992 Pergamon Press Ltd

Primed in Great Britain .

A RE-APPRAISAL OF A CASE OF PERSISTENT GLOBAL AMNESIA FOLLOWING RIGHT TEMPORAL LOBECTOMY : A CLINICO-PATHOLOGICAL STUDY ELIZABETH K . WARRINGTON and LEO W . DUCHEN National Hospital for Neurology and Neurosurgery, Institute of Neurology, Queen Square, London WCIN 3130, U .K . (Received 7 October 1991 : accepted 15 January 1992)

Abstract-We report a reappraisal of patient NT who became severely amoebic after a right temporal lobectomy for intractable epilepsy (DnsDALE et a! ., Neurop,eyehnfogia 1,287, 1964 [6]) . Histological examination, albeit incomplete, indicated that there was no abnormality in the receded temporal lobe . At autopsy a sclerotic lesion of the unoperated left hippocampal formation was found . This case is therefore not an exception to the general rule that a severe and global amnesic state is only observed with bilateral lesions . Her performance on a wide range of memory tests is shown to be indistinguishable from patients with an amnesic syndrome due to KorsakulT's psychosis .

INTRODUCTION THERE ARE a number of critical lesion sites that give rise to global memory deficits . However, it is generally accepted that severe amnesic states arc only observed in patients who have sustained bilateral damage [5, 7, I1] . Unilateral ablations of the temporal lobe involving the hippocampus do, although rarely, give rise to severe global amnesic states . In these cases one supposition is that there was undetected damage in the intact temporal lobe [11] . The alternative proposition that the amnesic syndrome can result from a strictly unilateral lesion was advanced by DIMSDAT .E et aL [6] . They described a patient in whom a right temporal lobectomy had been performed in 1961 for the treatment of focal epilepsy . This resulted in a severe and persistent amnesic state without general dementia . Pre-operative and postoperative eleetro-encephalography, air encephalography and angiography all failed to provide any evidence of a lesion in the left hemisphere . They speculated that in this case and in a small proportion of other patients undergoing unilateral temporal lobectomy, anatomical substrates of memory functions are atypical in being lateralized to one temporal lobe, the temporal lobe that has been ablated . Hence the devastating amnesic syndrome . NT ., the patient described by DIM5DALE et a( . [6], was subsequently studied intensively in the Psychology Department of the National Hospital and featured as the "temporal lobe case" in a number of experimental studies reported by Warrington and her colleagues between 1968 and 1978 . N .T . died at the age of79 in 1986 . In this report we provide a detailed account of her cognitive skills and amnesic syndrome together with the post-mortem data .

CASE REPORT N .T . (d,o,b. : 1907) was a right-handed housewife whose first admission to Maids Vale Hospital was in December 1960 for investigation and treatment ofepilepsy . Her first grand-mat seizure had occurred 28 years previuusly at the 437

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E . K . WAMMPGTOR and L . W . Ducties

age of 25 and these had increased in frequency as had her frequent partial seizures . On examination there were no neurological signs of note . However, on neuropsychological assessment a selective verbal memory deficit was observe[ . Preoperatively a right carotid arteriogram was performed and apart from some slight narrowing of the lower end of the internal carotid, no abnormalities were detected . Ventriculography demonstrated some minor abnormalities affecting the right frontal horn and the roofs of the bodies were a little irregular . The critical investigation was electro-encephalography which provided consistent evidence of a right anterior temporal focal abnormality . A formal right temporal lobectomy was carried out in January 1961, the posterior incision lying 6 cm from the tip of the temporal lobe . The incision was extended into the temporal horn and the lobe removed with Ammon's horn . The onus and amvgdala were also removed . Her post-operative condition was described by DIMSDALE era! . [6] as follows : "For the first three post-operative days she was drowsy and with no spontaneous conversation, although she was easily roused and co-operative and replied to questions and commands . On the third post-operative day she was pyrexial and complaining of headache- lumbar puncture revealed blood-stained ('SF . This was interpreted as a secondary haemorrhage into the cavity and was treated with repeated lumbar puncture . The haemorrhage appeared mild and was not accompanied by any obvious change in consciousness or by motor symptoms . As she became more spontaneously talkative during the week following the operation, confusion and amnesia became clinically obvious although she continued to remain comparatively well orientated for time and place ." A left carotid arteriogram which was performed 15 months post-operatively was entirely normal as were the appearances of the left cerebral hemisphere with Ventriculography . Further details of the case history and of the neurological investigations are given by DIMSDALQ et at. [6] .

Neurops ychological Investigations Cognitive abilities . N .T . was originally tested pre-operatively on the full WAIS and post-operatively on a shortened version of the WAIS . Her verbal and performance IQ figures from the same seven subtexts, on each occasion, are given in Table 1 . At a later date (1973) she was tested on Raven's Progressive Matrices and scored 32/60 which has an IQ equivalent of 110 . Table I . Verbal and performance intelligence test scores : serial testing

December 1960 April 1962 April 1967 July 1975

VIQ

PIQ

101 99 103 100

99 93 99 88

Short-term forgetting . The Brown-Peterson paradigm was used to assess short-term forgetting . N .T . was a subject in the BADDELEY and WARRINGTON [I] experiment testing recall of three words after delays of 1, 5, 10, 30 and 60 sec during which she performed a distracting task . NT's performance on this task was very similar indeed to a group of agematched control subjects (see Fig . 1) . Retrograde amnesia . N.T . was able to provide accurate basic autobiographical details going hack to her schooldays . She had however considerable difficulty elaborating and providing details . For example, she was very unclear about what she had done in the war years even though she lived in London during the 1939/40 period . N .T . was one of the patients in the SANDERS and WARRINGTON [13] investigation of retrograde amnesia . They devised a test of past public events and a test of memory for well-known faces . The events spanned a time period of nearly 40 years and the famous faces were people prominent in the public domain going hack for 25 years . There was a recall and recognition version of each test . NT's scores (tested on 5 .8 .69), for each time period sampled, together with the agematched control group scores on the events questionnaire, are given in Table 2 . NT's performance on the two versions of the Faces memory test (29 .4 .70) are shown in Fig . 2 . On



AMNESIA

WITH

UITFMPORAL nuItOLOCY

01)1 S 5

439

30 DELAY (sets)

Fig. t . Recall scores for N .T. and control subjects for three words as a function of delay using an intervening dsstractiag task .

Table 2 . Recall and recognition scores for N .T . and control subjects for public events for each time period sampled Recall NJ . Controls Recognition NT . Controls

1968

1965

1960

1955

1950

1945

1940

1935

1930

2 7 .7

0 7 .1

0 3 .8

0 4.8

0 5 .0

0 5 .2

0 6.2

0 4.5

0 2 .6

5 10 .4

5 9 .8

4 8 .0

5

6 8 .1

3 8 .7

RETROGRADEAMNESIA Memory for faces Recall s-aConhds ooNS

O Cs

lOs

9

16

RETROGRADE AMNESIA Memory for faces

14 T12

MCIXIIIVIS

ooN.T

8 6 z4 2 r Caewpay

s 1940s

195ps 195 s T~IOs

Fi_e. 2 . (a) Recall scores; (b) recognition scores for N .T . and control subjects for well-known faces for each time period sampled .



440

E. K .

WARRiruc:TON

and L . W . Demur;

the recall version of both the questionnaire and famous faces test her performance is at floor level ; she was virtually unable to recall any information from any time period sampled . On the recognition version of each task she scored close to a chance level for all time periods sampled . These findings document a profound retrograde memory loss extending into the remote past . Ant erograde amnesia . N .T . had a profound deficit for on-going events . She usually failed to recognize the Psychology Department (a distinctive hut) or the psychologist who spent many hours testing her. On recognition memory tests for words and faces she scored below the 5th percentile on both recognition memory for words (35/50 correct) and for faces (25/50 correct) . On a similar recognition memory test for distinctive coloured pictures she scored 29/50 correct [I6] . N .T . was one of the patients in an experiment that compared different methods of testing retention [18] . Ten word lists were presented and retention was tested by recall, yes/no recognition, cuing with either the first three letters of a word and prompting with a fragmented, degraded word stimulus . N .T . was significantly impaired on the recall and yes,/no recognition tasks and scored within the normal range on the two "cued recall" tasks (sec Fig . 3) .

METHODS OF TESTING RETENTION 20

®Controls

~N .T. X15

E0 U

~,10 E3 Z



IluLlul

Recall

Recogtitionc

.

Frog ented rd

Fig . 3 . Recall scores for N .T . and control subjects using four different methods of testing retention .

Effects of cognitive mediation . N . F . was a subject in the experiment that explored different types of cognitive mediation in amnesic patients [2] . It was reported that the amnesic group (n=6) as a whole (that included Korsakoff cases) were able to obtain some gain from phonemic and semantic clustering in words to be remembered, but they failed to show any gain from visual imagery, a condition beneficial for normal subjects . NT's scores on each experimental and control test together with the control group scores are given m Fig . 4 . N .T . showed the typical amnesic pattern in that there was no gain from visual imagery, a condition on which her performance was particularly poor, and additionally she obtained a near normal score on the acoustic clustering condition . Perceptual learning

(1) There is a general consensus that perceptual learning can be intact in patients with a denseamnesie syndrome . An early demonstration of preserved memory was amnesies' ability to learn to recognize and retain fragmented drawings of common objects [17] . N .T . was the



44 1

AMr ESIA WITH HITGMPORAL PATHOLOGY

80 70 60 0

U

50

cn

40

C:

30

a u C,

20 10 0

C

I

1

I

I

I

E

C

E

C

E

Phonemic Clusters

Visual Imagery

Semantic Clusters

Fig . 4 . Recall scores for the control list (c) and the experimental list (c) for N .T . and control subjects using three different manipulations of cognitive mediation . first amnesic patient to be tested using this technique . Her error score on each trial of each day of testing and mean score of the control group are given in Fig . 5 . N .T .'s performance is only marginally weaker than that of the control group and there is clear evidence of day to day "savings" .

20 18 ° 16 14 12 ,n 10

pER~EPTUAL LEARNING Gellin Pictures .-.Controls 0-ONT

PS Lb6

4 O.

0 1 2 3 4 5 Day 1

1 2 3 4 5 Day 2

O

123 Day S

Fig . 5 . Error scores for N .T . and control subjects on Golhns Incomplete Pictures, on five trials on three successive days . (2) N .T . was tested on the pictorial version of the McGill anomalies test . On the first 20 items she scored only three correct. For those items she failed, the anomaly was pointed out to her . A further five trials were administered on the same day and an additional trial after a 24-hr delay . She demonstrated good learning in that after four trials her performance was nearly error-free and she demonstrated good retention after 24 hr (sec Fig . 6) . Subsequently, she was tested on 20 new items, she scored 6/20 which is close to her original baseline score . Word completion experiments . N .T . was a subject in all the word completion experiments reported by Warrington and Weiskrantz between 1974 and 1978 . In these experiments they



44 2

E. K.

WARRINGTON

and L . W .

DCriruN

PERCEPTUAL LEARNING (NT) McGll Anomalies -o

1 2 3 456"? Trial Number Fig. 6. Number correct score for N .T . on the McGill anomalies test on six consecutive trials and one

7A-hr delay trial . presented subjects with printed lists of words and tested their retention by presenting the first three letters of the target items and requiring the subject to complete the target word . In summary N .T . obtained scores that indicated significant retention albeit at a somewhat lower level than the age-matched controls . One of these word completion experiments manipulated the number of available response alternatives, word concreteness and number of learning trials [19] . NT's percent correct score, together with age-matched control groups' mean scores for each condition of this experiment, are shown in fig . 7 .

1009o 80 70 60 50

Narrow

Wide

I

r

Concrete

Abstract

r 1 Trial

3 Trials

Fig . 7 . Recall scores for N .T . and control subjects for word completion using lists that manipulated

the number of response alternatives, word concreteness and number of learning trials . Response alternatives can be effectively eliminated by using as stimuli, common words that are uniquely specified by their first three letters (e .g . juice, onion, aunt, etc .) [201 . Subjects were first asked to generate a word given the first three letters from a pool of 200 "unique" words . The test list comprised the first 20 words for which the subject failed to generate a response . The subject then copied the correct words and then read them aloud . Retention of the critical 20 words was tested after a 24-hr delay by representing the first three letters and asking the subject to complete the word . The mean correct score for the control group was 9 .5%20 ; N .T . scored 12%20 correct . Neonnpat Joshoyfcal findings

NT . died in September 1986 at the age of 79 and the post-mortem examination was done 48 hr after death . Outside the nervous system the main pathological changes were found in the cardiovascular system . There was



AMNESIA WITH Hit 5tMIPORAh PA'T'HOLOGY

44 .3

generalized severe alheroma affecting especially the coronary, carotid and cerebral arteries and aorta . There was extensive old myocardial infarction of the left ventricle and death had resulted from left-sided cardiac failure causing large bilateral pleural effusions . The left common and internal carotid arteries were severely atheromatous, calcified and almost completely occluded . .VeuropaUmlngy . The skull bones were thick and dense with dura densely adherent to bone . An old defect of the right temporal lobe was apparent, the site in the middle tolls being occupied by a cystic cavity lined by a thick smooth membrane . After fixation the total brain weight was 904 g, that of the brain stem and cerebellum being 124g . Cerebral vessels of the circle of Willis showed patchy atheroma . The right temporal lobe had been removed exposing the cerebral peduncle on that side . The lobectomy had included the uncus . all of the hippocampal formation hack to the tail which was shrunken, the remnant being seen at the level of the selenium of the corpus callnsum . The white matter of the temporo-occipital region was cavitated and the cavity lined by grey soft tissue . The margins of the operative defect were irregular and slightly brown in colour . It was estimated that 5-6 cm of temporal lobe had been removed . Corona) slices showed a slight dilatation of lateral ventricles, more marked on the right . There were old needle tracks in both parietal regions . Of the right temporal lobe only some of the posterior part of the superior temporal gyms remained in addition to the must posteriorpart of the tail of the hippocampus . The right fimbria and fornix were shrunken and grey and the posterior part of the corpus eallosum was thinner than normal . The left hippocampus (Fig. 8a) was smaller than normal (Fig . 8b) and the angle between the alveus and the floor of the temporal horn was more than 80" instead of the usual I S 20' . The grey matter of the hippocampus was pale and reduced in amount . The right mamillary body was markedly shrunken but even the left mamillary body was smaller than normal . In the brain stem the right cerebral peduncle and the right side of the pons were slightly smaller than the left . The aqueduct was patent, substentia nigra was normally pigmented and there was no obvious asymmetry of pyramids, olives or cerebellar hemispheres . Histulogkol exoonooGon . The sections of the right temporal lobe removed at operation in 1961 were reviewed (courtesy of Dr R . O . Bernard). Several blocks of the convexity and deeper structures including the amygdaloid complex were examined with routine staining methods and were within normal limits . Only a small part of the hippocampus was seen in the sections, including a short length of dentate fascia, some end-folium (CA4) and fragments of pyramidal cell layer the site of which could not be determined . Apart from surgical artefact, the hislological appearance of these regions were all within normal limits_ Blocks were taken from many regions of the left and right hemispheres, brain stem, cerebellum and spinal cord . They were embedded in paraffin wax and sections stained by routine neurohistologieal techniques including luxol fast bloc-cresyl violet for myelin and silver impregnation for axons by the modified Glees method . The le( hippocampal,Jartnation was examined at four levels and was very abnormal in all (Figs 9-Ill . There was severe reduction in numbers of pyramidal cells of ('Al 4 . At all levels CA2 was almost totally depleted of neurons (Fig . 10), only an occasional cell remaining, together with astroeyles . No macrophages were present . Cells of CA 1 were relatively preserved . CA3 neurons were present in patches and those of CA4 much reduced in number, especially pnsteriorly where very few remained . The granule cells of the dentate fascia (Fig It) were much reduced in number particularly in its dorsal part at all levels antero-posteriorly . Alveus fimbria and fornix contained wellpreserved myelinated fibres in abundance compared with the right side, but when compared with the normal were reduced in bulk . There were no lesions identified in the left temporal lobe such as cortical dysplasia or heterotopias . Many of flue surviving pyramidal cells in CAl contained granulo-vacunlarinclusions and there were occasional neurons in this area as well as in the subieulum which contained neurofibrillary tangles . Moderate nmtthers of oeuritic plaques of the senile type and some deposits of amyloid were also present . The right mamillary body was very small and contained few neurons . The left mamillary body contained a moderate number of neurons, clearly more than the right but less densely packed than normal . No clear-cut differences were identified between the two sides of the thalamus, particularly the anterior and dorm-medial nuclei which were heavily gliosed on both sides . Other changes in the hemispheres included several scattered small cortical infarctions which were of fairly recent origin containing abundant lipid macrophages arid lined by reactive astrocytes and blood vessels, and there were perivascular rarefadions particularly marked in halal ganglia . These were in keeping with small-vessel atherosderosis . In the brain stem, the subslantia nigra and locus ceruleus were normal but there were abnormalities in the pontine nucei on the right . Groups of neurons particularly in the ventral part of basis ponds were small and closely packed compared with those on the left . These changes were interpreted as transneuronal in nature .

DISCUSSION N .T . underwent a unilateral right temporal lobeetomy for intractable epilepsy that resulted in a severe and unremitting amnesic state . At autopsy a sclerosing lesion in the supposedly intact left hippocampal formation was observed .



434

F . K . W4 RRINGTON and L . M/ . DccimN

Although no abnormality was found in the resectioned specimen of right temporal lobe there cannot be complete certainty that the reflected tissue was entirely within normal limits because of the limited amount of hippocampal formation seen histologically . Some short lengths of pyramidal layer, fascia dentata and CA4 area were seen and these were without abnormality . Most components of the remaining, left, hippocampal formation were abnormal throughout its length and with the degree of cell loss observed, any fragment of it would have looked clearly abnormal had it been removed surgically . Determining the age of old inactive cerebral lesions is difficult . It can be said, however, that the changes in the remaining left temporal lobe were of very long standing . There was no suggestion of any persisting reaction to cell necrosis such as could have been caused by recent hypoxic damage . If an hypoxic episode such as severe hypotension or cardiac arrest occurring post-operatively were to he postulated as a cause of damage to the remaining hippocampal, damage to other vulnerable areas of the brain such as boundary zones in the cerebral cortex and cerebellum would have been most likely [3] . The absence of such extrahippocampal lesions due to hypoxic, and the rapidity with which the amnesic state developed indicate, we believe, that the hippocampal sclerosis on the left, typical of temporal lobe epilepsy in many eases [4 . 10] antedated the loheetomy operation but was not identified at the time . The other neuropathologieal findings are considered to he secondary to the loheetomy (transneuronal atrophy of the mamillary and pontine nuclei) or more recent in onset (atheromatous disease of cerebral vessels and plaques and tangles typical of senile changes, or early Alzheimer's disease) . It cannot be considered as at all likely that these abnormalities played any role in the rapidly developing amnesic state . Thus N .T . was not an exception to the orthodox view that a bilateral lesion is an invariant condition in the aetiology of a severe amnesic state . At any rate the speculation that NT's functional deficit reflected a possible, albeit atypical, cerebral organization of memory functions is not upheld . There is as yet no evidence that "the amnesic syndrome can result from a strictly unilateral lesion" [II] . Two further issues merit comment : The WADA technique in which sodium amytal is injected into the carotid artery has the temporary effect of unilateral suppression of function was initially used to determine lateralization of language functions . Although it was acknowledged that bilateral surgical procedures would compromise memory functions, the risk from unilateral ablations was uncertain . MILNIX [11] pioneered the use of the WADA technique for establishing whether after temporal loheetomy the eontralateral hemisphere could subserve normal memory functioning . Memory tests were therefore incorporated into the examination of language functions . Evidence of transient amnesia following suppression of the ipsilateral hemisphere would be a contra-indication for surgical intervention_ The evidence of an undeclared lesion, in the case of N .T . sufficient when combined with the surgical ablation to result in a grave amnesic state, serves to emphasize the importance of screening for memory functions in addition to language functions in all candidates for surgery . In a series of papers from 1968 to 19Th Warrington and Weiskrantz reported group data for small numbers of amnesics, including N .T . and patients with Korsakolfs psychosis . It has been suggested that this procedure would mask distinctive patterns of performance in the individual case . A clinico-pathological study of two of their Korsakoff's psychosis cases with severe amnesic states has been reported [9] . In the brains of both patients there was "marked gliosis, shrinkage, and unusual colouration in the mamillary bodies . . . in addition, in both

AMNESIA WITH 9ITEMPORAL PATHOLOGY

Fig . S. The left hippocampal formation of N .T. (a) is shown in coronal section at the level of the pulvinar of the thalamus . It is shrunken and the definition of its component structures particularly of the pyramidal layer (arrow) has been lost . A normal hippocampus of a case without neurological disease is shown in (b). Note the difference in shape of the temporal horns .

445



44 6

E . K . WANRINGION and L . W . DocnuN

Fig . 9 . Corona) section of the left hippocampus of N : f . (a) shows marked atrophy of most of the pyramidal layer (arrows) and end folium, and severe reduction in amount of myelinated tissue in alveus and fimbria compared with a normal control case (b) . Luxol fast bloc-cresyl violet x 6 .

AMNESIA WITH BITFMPORAL PATHOLOGY

Fig . 10 . Part of area CA2 of pyramidal cell layer of left hippocampus of N .T. (a) . One neuron only is seen, remaining nuclei are of astrocytes . Compare with pyramidal cell population of CA2 of a normal brain in (b) . Luxol fast blue-cresyl violet x 120 .

447



448

E . K . WARRINGTON

and L . W .

DUCHEN

Fig . 11 . Dentate fascia of N .T . (a) and normal brain (b) . Note marked loss of granule cells from (a) . Luxol fast blue-cresyl violet x 120 .

AMNESIA \VITH RITEMPORAL PATHOLOGY

449

there was a thin band of gliosis bilaterally between the wall of the third ventricle and the medial dorsal nucleus of the thalamus, its rostral limit lying anterior to the medial dorsal nucleus" . The amnesic states of these two Korsakoff patients may be compared with the present case, N .T . It has been proposed that there are fundamental differences between amnesic states due to temporal lobe lesions that involve the hippocampus and those involving dicnccphalic structures, especially the thalamus and mamillary bodies . It has been suggested that medial temporal lobe cases have a major deficit in the acquisition of new information in whom by comparison old memories are well preserved [15, 12] . This anterograde greater than retrograde formula does not apply to N .T . Her retrograde amnesia was dense and she scored at floor level at all time periods sampled on our quantitative measures . In this regard her performance was indistinguishable from the two Korsakoff amnesics who were tested on the identical events questionnaire and famous faces test [9] . As an aside it was N .T . who alerted one to the dubious procedure of estimating the duration of the retrograde amnesia from "time tagged" questions . To one item on the event questionnaire "Which Queen came to England at the beginning of the war", she replied Queen Boadicea . A further but more problematical differentiating characteristic of the two aetiologies of the amnesic state are the "forgetting rates" which are supposedly more rapid in the temporal lobe cases [8, 14] . Indeed, despite several periods of daily contact, N .T . did not acknowledge that the experimenter was familiar . Both the two Korsakoff cases and N .T . were able to learn to criterion using word completion and perceptual learning procedures . With retesting and relearning significant "savings" were demonstrated in all three patients . N .T . like the two Korsakoff cases scored within the normal range when tested after 24 hr on a word generation task . Our conclusion is that N .T . is not an exception to the bilateral "rule" . She became profoundly amnesic after a unilateral right temporal lobectomy and at autopsy an atrophic lesion in the left hippocampus was found . Both qualitatively and quantitatively her performance is very similar indeed to that of two Korsakoffs with lesions in the mamillary bodies and thalamic nuclei . Our findings provide no positive evidence of there being fundamental differences between amnesic states due to lesions in the dicncephalon and medial temporal lobe structures . We should like to thank Frances Mott for the histological preparations and Stephen Durr for the photographs . We should also like to record our indebtedness to the late Dr R . T . C . Pratt who initiated the stud v of NT's memory deficits and whose continued interest in this case made the present study possible . Acimowledgernents

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7 . DUYCK .AERI S . C., DEROUESNY, C ., SIGNORE r, J . L ., GRAY, 1*, EsrrouROLLE, R, and CASTAIGNE, P . Bilateral and limited anrygdalohippocampal lesions causing a pure amnesic syndrome . Arm . Neural 18, 314-319, 1985 . 8. HtrarrRT, F . A . and PIECY, M . Normal and abnormal forgetting in organic amnesia : Effect of locus of lesion . Cortex 15, 385-390 . 1979 . 9 . MMtt, W . G . P ., WARRINGTON . E . K . and WGISKReWTZ, L. Neurupalhological and psychological examination of two patients with Korsakolf's psychosis . Brain 102, 749-783, 1978 . 10 . MARGERESON, J . H . and CORSFLLIS . J . A . N . Epilepsy and the temporal lobes . Brain 89, 499 530, 1966 . 11 . MILNER, B . Amnesia following operations on the temporal lobes . In Amnesia . C . W . M . WntrrY and O- ZANGWtLL (Editors'), pp . 109-I33. Butlerworth, London, 1966 .

12 . 13 . 14 . 15 .

PARKIN, A . J. Amncsic syndrome : a lesion-specific disorder. Cortex 4,479 508, 1984 . SANDERS, H . l . and WARRINGrON, E . K . Memory for remote events in anmesia patients . Brain 94, 661 668,1971 . SQUIRE, L . R . Two forms of human amnesia : An analysis of forgetting . J . .Nemnsei . 1,635-640, 1981 . SQUIRE, L . R . and COHFN, N . J . Remote memory, retrograde amnesia and neuropathology of memory . In

Human Memory and Amnesia, L . CERMAK (Editor), pp . 275 303 Lawrence Erlbaum, Hillsdale . 1982 . 16 . WARRINGTOS, E . K . Recognition memory lest . NFER-Nelson . Windsor, 1984 . 17. WARRINotoN, E . K . and WEISKRANTZ, L . New method of testing long-term retention with special reference to anmesic patients. Nature (Gold.) 277, 972 974. 1968 . 18 . WARRINGTON, E . K . and Wet5KRAN-rz, L . Amnesic syndrome : consolidation or retrieval . Nature (Loud .) 228, 628-630, 1970 . 19 . WARRINGTON, E. K . and WFISKRANTZ, L . The effect of prior learning on subsequent retention in amnesic patients . Neuropsychologia 12, 419-428, 1974 . 20 . WARRING ION, F . K . and WEISKRANT/, I . . Further analysis of the prior learning effect in amnesic patients . Neuropsycholagia 16, 169-177, (978 .