test4 · calabrese, markowitsch, dunven, widlitzek, haupts, holinka, gehlen figure3...

34ournal ofNeurology, Neurosurgery, and Psychiatry 1996;61:304-3 10

Right temporofrontal cortex as critical locus forthe ecphory of old episodic memories

P Calabrese, H J Markowitsch, H F Durwen, H Widlitzek, M Haupts, B Holinka,W Gehlen

AbstractA 54 year old patient of average intelli-gence with a severe and enduring loss ofold autobiographical memories after her-pes simplex type 1 infection is described.She was tested with a comprehensive neu-ropsychological battery two years after theinfection. Special emphasis was laid onexamining different aspects of retrogradememory. The neurological examinationinvolved MRI and SPECT. Brain damagewas found mainly in the right tempo-rofrontal region, but minor left sided dam-age to this region seems possible. Thepatient was in the normal or slightly sub-normal range for all tested anterogradememory functions, but manifested severeretrograde memory deficits with respect toepisodic old memories and more moderatedeficits in tests of general knowledge(semantic old memories). It is concludedthat the ecphory of old autobiographicalmemories relies heavily on an activation ofthe right lateral temporofrontal junctionarea, but that probably only some comple-mentary left hemispheric damage to theseregions will lead to major and persistentretrograde amnesia. Alternatively, the dis-connection between major prefrontal andposterior cortical regions may provide abasis for retrograde amnesia.

( Neurol Neurosurg Psychiatry 1996;61:304-3 10)

NeurologicalUniversity Hospital,Bochum-Langendreer,GermanyP CalabreseH F DurwenM HauptsB HolinkaW GehlenPhysiologicalPsychology, Universityof Bielefeld, Bielefeld,GermanyH J MarkowitschInstitute of Radiology,University Hospital,Bochum-Langendreer,GermanyH WidlitzekCorrespondence to:Dr Hans J Markowitsch,Physiological Psychology,University of Bielefeld, POBox 10 01 31, D-33501Bielefeld, Germany.Received 8 December 1995and in revised form12 March 1996Accepted 12 March 1996

Keywords: retrograde amnesia; memory; medial temporallobe

In recent years evidence for an anatomical dis-sociation of anterograde and retrograde mem-

ory functions has accumulated.'-'0 While theessential bottleneck structures, relevant forinformation transmission for long term storagehave largely been established," there is still a

substantial lack of consistency with respect tothe brain regions implicated in focal retrogradeamnesia.5-7 1213 The structures most often impli-cated in focal retrograde amnesia are situated inthe prefrontal and temporal cortex, with some

authors emphasising the importance of one

structure or the other, and other authorsassuming that only the combined and bilateraldamage of portions of both frontal and temporalregions are necessary for the appearance of a

fullblown retrograde amnesic syndrome.'3 Thisinconsistency is enhanced by the currentlywidely accepted dissociation of different mem-ory systems of which the episodic semantic dis-

tinction is the most common one.'4 Episodicmemories are those which can be traced backwith respect to time and locus, whereas seman-tic memories signify those of a general nature(knowledge of the world).

In a recent review,'3 the hypothesis that thecombined action of inferolateral prefrontal andanterolateral temporal cortices is necessary forthe retrieval of long term memory, wasadvanced on the basis of a comparison of sev-eral case reports and data on memory retrievalin normal subjects obtained with PET.Furthermore, it was speculated that theseregions in the right hemisphere would primarilybe engaged in triggering episodic old memories,whereas the same regions of the left hemispherewould be involved in retrieving informationfrom the knowledge system.'3 We report thecase of a patient who fits into this proposedscheme by being selectively retrogradelyamnesic in the episodic memory domain andhaving a SPECT documented hypoperfusion inthe right temporo frontal junction area.

Case reportThe patient, a 54 year old right handed womanhad been admitted three years ago to the hospi-tal as an emergency case with herpes simplextype 1 meningoencephalitis.

NEUROLOGICAL AND NEURORADIOLOGICALEVALUATIONThe history of her illness started with com-plaints of nausea and tiredness one week beforeadmission. Two days before admission shedeveloped high fever with temperatures up to39 8°C, complained about increasing head-aches, and became more and more disoriented.Intermittently she was unable to recognise herfamily and showed signs of visual hallucinationsfor short periods. Finally she drifted into a stateof severe drowsiness.Her previous medical history involved left

sided mastectomy for breast cancer as well as ahysterectomy, both about 10 years earlier. Thefamily history of the patient disclosed no eventswith neurological, psychiatric, or other rele-vance.On admission she was in a severe drowsy

state, but could be awakened by painful exter-nal stimuli. She was then able to answer simplequestions with yes or no, and to carry out simplemovements to verbal command. A more com-plex form of communication, however, was notpossible. Further neurological examination dis-closed soft meningeal signs as well as a discreteto moderate left sided hemiparesis including

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Right temporofrontal cortex as critical locus for the ecphory of old episodic memories

Figure I General TlweightedMRI after GdDTPA contrast injectionperformed about three yearsafter infection. Coronalsections from top left tobottom right demonstratethe principal loci of braindamage in the right inferiorlateral prefrontal cortex(top left), the righttemporopolar cortex (topright), and the rightanterior temporal lobe(bottom left and right).

bracchiofacial hemiparesis. Babinski's sign waspositive and the muscular reflexes were raisedon the left. Reactions to painful stimuli couldbe elicited from both sides to the same extent.An initial cranial CT showed a hypoattenua-

tion in both hemispheres with a discrete rightsided accentuation, predominantly in the fron-totemporal region. After injection of an intra-venous contrast a diffuse inhomogeneousenhancement was seen in the areas affected. Acranial CT control, one month later, was nor-mal.The first MRI was performed somewhat less

than three months after onset of the disease.

There was low signal intensity on Ti weightedimages and high signal intensity on T2weighted images in the right frontotemporalregion with the maximum in the right temporallobe, and, in addition, there was evidence of acircumscribed cystic substance loss in the righttemporal and frontobasal brain regions. Thedamage included anterior portions of the rightamygdalohippocampal region and affected inparticular the region of the pathway of the rightventral branch of the uncinate fascicle (fig 1 inMarkowitsch"3). Results from a second MRI,performed about three years later, confirmthose of the first (figs 1 and 2). Minor left sided

Figure 2 Axial protondensity images through thecentre of the patient's braindamage, taken about threeyears after infection. Notethat the extent of the braindamage closely follows thecourse of the ventralbranch of the uncinatefascicle.



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Figure 3 99m Tc ECD SPECT sections, taken about three years after infection. Axial (top row), coronar (middle row), and right and left sagittal sections(bottom row) show the area ofhypoperfusion in the right temporofrontal region.

frontotemporal brain damage seems possible(figs land 2).An ECD SPECT, performed in the initial

phase of the disease, showed a pronouncedhyperperfusion in the right frontotemporalarea. After three months, a control SPECTstill showed a moderate hyperperfusion in thesame region, whereas a control, done threeyears later, showed an area of circumscribedhypoperfusion in the same location (fig 3).

Initial EEG recording showed a moderatebut generalised slowing of the backgroundactivity as well as a theta/delta focus in theright temporoparietal region. Furthermore,intermittent epileptogenic activity charac-terised by single sharp waves, was recorded inthe same area, without clinical evidence ofepileptic seizures during her stay in hospital.After six months the EEG recording was com-

pletely normal.Analysis of CSF showed a white cell count

of 840/3 cells and a protein level of 58 mg%.The serological data showed positive findingsof IgG and IgM antibodies to the herpes sim-plex type 1 virus. Values for CSF became nor-

mal six months after onset of the disease.

NEUROPSYCHOLOGICAL EVALUATIONTesting was performed two years after theinfection. The neuropsychological tests and a

summary of the results are listed in the table.They included tests of intelligence, attention,concentration, language, cognitive flexibility,and various forms of memory tests. Most ofthese tests have been used and described indetail in previous publications.2 131516The patient was alert and motivated. She

took part in conversations, was socially welladjusted, and was able to interact in variousways. When instructed, she could rememberto do something or to go to a certain place. Informal testing, she gained an IQ of 103 points,and her attention was in the normal range. Inthe Wechsler memory scale R she was in thelower average range (general memory index 93points). Other tests of verbal and non-verbalanterograde memory confirmed the impres-sion of her normal to somewhat sub-averageanterograde memory abilities. Her cognitiveflexibility was below average.

RETROGRADE MEMORYThe patient described herself as lackingepisodes of her personal past from severaldecades before her brain infection. We usedthe following tests to determine her perfor-mance level in the domains of retrogradeepisodic and semantic memory: the autobio-graphical memory interview (AMI)17 and theCrovitz form test4 were given to assess her



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Right temporofrontal cortex as citical locus for the ecphory of old episodic memories

Neuropsychological tests used and main test results

Normative datalAssessedfunction and test Patient Control subjects

Intelligence 103 100 (SD 15)Attention:

d2 Concentration-endurance test 32%ile 25%ile-75%ileTrail making test, form A 50%ile 50%ile

Language:Token test 95%ile

Cognitive flexibility:FAS verbal fluency test 16 (cut off 17)Trail making test, form B 83 (25%ile) 50%ileProactive interference 7, 6, 4, 4, 4*

Learning and anterograde memory:Digit span forward 6 5-6Digit span backward 4 4-5Corsi block span forward 5 5Corsi block span backward 4 4-5Wechsler memory scale-R

Attention/concentration index 87 100Verbal memory index 99 100Visual memory index 88 100General memory index 93 100Delayed recall 86 100

Rey auditory verbal learning testTrial 1 6 6-4Trial 2 7 8-2Trial 3 9 10-2Trial 4 9 11 1Trial 5 11 11-6Distractor (list B) 4 4-6List 6 7 9.9Delayed recall 7 10-2

Rey complex figureCopy 35 3530 minute delay 18 18-8

Retrograde memory:Autobiographic memory interview'7

Personal semantic events(childhood, adulthood, recent) 14, 12-5, 18 21, 20, 21Autobiographical incidents(Childhood, adulthood, recent) 1, 2, 7 8, 9, 9

Crovitz test (10 words per time period)4 See fig. 4Famous faces testt 27% 42%Semantic general knowledge test5"16 71 > 92

For the Rey auditory verbal learning test and the Rey complex figure means are given afterSpreen and Strauss'8; for the AMI the scores are given for a control subject of comparable age(taken from Weniger et al9).*Although the number ofremembered items is not atypical, the release from proactive interference(4, her last score) is below average.tSee fig. 5.

episodic retrograde memory, and for testingher general knowledge the semantic generalknowledge test of Schmidtke'5 16 and a famousfaces test'215 were used. The AMI consists of asemistructured interview covering all epochsof a subject's life; it is subdivided into twoparts covering the more general, semantic, andthe personal events domains. In the Crovitzform test 10 high frequency nouns are admin-istered and the patient is asked to describepersonal experiences and unique episodesrelating to each word. The instructions were:

Figure 4 Perfornance ofthe patient in the Crovitztest. Out of 10 possibleresponseslperiod, thepatient was able to giveonly three or two for herearliest decades, and fivefor the period after theinfection.

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Time periodFigure 5 Famous faces test; 15 faces were presented!period. Here, the patient was less impaired than inautobiographical memory, but nevertheless showed a timegradient which reflects the onset of the infection in 1993.

"Relate personally experienced life eventsfrom any time period evoked by each of thefollowing words . . .", and "Now estimate thedate of its occurrence." The semantic generalknowledge test uses 100 items of the kind"What is the name for the child of a cow?" or"What is the currency used in Switzerland?" Itfurthermore includes questions on geography,famous people, and animals, animal products,and attributes. The famous faces test con-tained per decade 15 portraits offamous people(sportspersons, politicians, actors, etc).By contrast with her abilities to learn and

remember new information, she had persistentand severe deficits in her old memory abilities.These were most prominent for her autobio-graphical past (fig 4), whereas her generalknowledge, measured with a famous faces test(fig 5) and the world knowledge test (and alsopartly reflected by the semantic part of theautobiographical memory interview) wasmuch less affected (table).

DiscussionOur patient is another in a series of severalpatients with a clear dissociation betweenanterograde and retrograde memoryabilites."21320 She also fits into a series ofpatients with combined damage of predomi-nantly temporopolar and inferolateral pre-frontal regions and focal retrograde amnesia.'3(Her brain damage included the right medialtemporal lobe as well, but we assume fromcomparing her case with previous ones12 l 3that the lateral temporal lobe regions are criti-cally implicated- in retrograde amnesia.)Furthermore, she corresponds to the proposedscheme of hemispheric specific retrogradememory disturbances"3: her brain damage ispredominantly right hemispheric and hermemory disturbances are largely in theepisodic memory domain. She also fits into thescheme proposed by Markowitsch"3 for theoccurrence of retrograde amnesia by havingbilateral (although mainly right sided) braindamage. The aetiology of her brain damage isnot unusual for patients with severe memory



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disturbances,20 21 including focal retrograde22amnesia.

This case therefore combines all features ofanatomicobehavioural interrelations for retro-grade episodic amnesia, as predicted byMarkowitsch's hypothesis." In addition, theoverlap between episodic and semantic distur-bances of old memories is in line with theassumption that these two memory systemshave to be viewed more as a continuum thanas sharply divisible entities: semantic informa-tion is generalised, repeated episodic informa-tion23 and the generalised (episodic plussemantic) deficiency of brain damagedpatients at the stage of memory encoding24may hold for the level of information retrievalas well, although it may be more distinct in thenon-damaged brain."3The episodic memory system is most likely

more sensitive to brain damage than theknowledge system: episodic information is

25unique, whereas semantic memories mayderive from episodic ones through generalisa-tion and repetition." Furthermore, episodicmemories for ecphory probably need a syn-chronised activation of affect coding structuresof the limbic system (amygdala).'6 (Ecphorydenotes the process by which retrieval cuesinteract with stored information so that animage or a representation of the information inquestion appears.)The temporopolar orbitofrontal junction

area will not be the locus of the engrams, butonly a necessary mediator."3 Although wefavour this region as the principal locus formemory ecphory, alternatively the disconnec-tion between major prefrontal and posteriorcortical regions may provide a basis for retro-grade amnesia. Retrograde amnesia is cer-tainly a multifaceted phenomenon which canaccompany various kinds of diseases andwhich can occur after damage to quite diver-gent brain loci. 1 2 4 27

ROLE OF THE FRONTAL CORTEX IN RETRIEVALResults from studies in patients with selectiveprefrontal damage usually do not indicate sig-nificant retrieval deficits. Instead, only theactive, effortful engagement in ecphorisinginformation may be disturbed.'8 Other fea-tures of mnemonic information processingwhich are altered after prefrontal damageinclude aspects of metamemory and memoryfor the temporal order of events.29 Further-more, the prefrontal cortex is viewed as actingin monitoring or supervising environmentalstimulation, or as applying strategies.'9

All of these functions have, however, acloser affinity to the dorsolateral than to theorbitofrontal aspects of the frontal lobes.Damage to this region is assumed to inducechanges in personality and emotional behav-iour.2930 Brazzelli et al"3 described a patientwith bilateral frontal and some additional cin-gular and temporal damage who had severeamnesia, most likely including a failure toretrieve old memories although formal testingof retrograde memory could not be accom-plished due to her incapacity to provide anykind of account. Recent 150 PET studies pro-

vide further evidence for a prefrontal involve-ment in verbal and pictorial episodic memoryretrieval."

In conclusion, the prefrontal cortex con-tributes to memory retrieval (or memoryecphory) both by providing the impetus ortrigger for an active search of the engrams(stored at other places and most likely in a net-work-like fashion"3) and by its capacity as atime sensitive organiser. As mentioned above,autobiographical memory is composed of per-sonally relevant and temporal knowledge. Thetemporal structuring or ordering of informa-tion is apparently necessary for its successfulecphory and retrieval. Results from singlecases with prefrontal damage strongly supportthis view."3" The patient's subnormal perfor-mance in all three tests on cognitive flexibility(and therefore a frontal lobe function) confirmthe view, expressed by Kopelman," that testresults in this domain are better predictors forretrograde memory performance than antero-grade memory tests.

ROLE OF THE TEMPORAL CORTEX IN RETRIEVALPenfield36 has elucidated many of the phenom-ena occurring during electrical stimulation ofthe temporal lobe. One of his findings was theappearance of what he called "psychicalresponses": reproductions of past personalexperiences which he attributed to the (lateral)temporal cortex. Recently Fink et al 26 similarlyfound with PET blood flow measurements astrongly increased activation in the anteriortemporal regions in response to ecphorisingautobiographical material. In summary, bothcase descriptions of epileptic patients withtemporal lobe involvement and functionalimaging data in normal human subjects indi-cate a role of lateral temporal portions inmemory retrieval. The anterolateral temporalcortex most likely provides the connection tothe posterior cortical centres of integrationand therefore to the major storage places ofthe engrams."7

EMOTION AND MEMORYSome studies point to emotional changes afterbrain damage. 15 38 39 The recent speculationthat the right hemisphere is principallyengaged in episodic memory retrieval and theleft in semantic memory retrieval,"3 is in linewith such a view as episodic memories areusually more emotional than semantic ones.Autobiographical information is probably rep-resented in a more complex way than semanticinformation and needs an involvement fromthe left language representing hemisphere aswell as from the right emotional one. The caseof an adolescent patient with automatic butnot consciously reflected memory retrievaldemonstrates this point.40

It is not unlikely that the ecphory ofepisodic, but not of semantic, memoryinvolves non-cortical limbic structures as wellas the cortical ones, which primarily representstored information."3 The basolateral limbiccircuit, composed of portions of the prefrontalcortex, the amygdala, and the medial thala-mus38 constitutes a basis for a network impli-



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cated in emotional memory processing.4 39 41The region of the medial thalamus can fur-thermore be regarded as a central gating sta-tion for consciousness42 and therefore for theactive, reflective processing, and associating ofold memories. The mediodorsal nucleus notonly projects to the prefrontal cortex, butespecially to those portions of the temporalcortex as well which are implicated in theecphory of old memories-namely, the tempo-ral pole (area 38)." On the corticocorticallevel, the temporopolar and the ventrolateralprefrontal areas are bidirectionally intercon-nected by the uncinate fascicle."3

Emotional flattening is a frequent concomi-tant in patients with retrograde amnesia, bothof organic and psychogenic origin."343 Takingall this evidence together, it is likely that dam-age to the temporofrontal junction areas mayresult in a blockade of access to storedengrams, particularly to those which requirean emotional flavour for ecphory as well.2526

WHY IS THERE SUCCESSFUL RETRIEVAL OFMEMORIES ACQUIRED AFTER BRAIN DAMAGEWITHOUT THE RIGHT TEMPOROFRONTALJUNCTION AREA?Patients with selective temporofrontal damageare still able to acquire new information longterm after the insult and subsequently recall itlong term. This recall must therefore occur viaroutes different from the damaged tempo-rofrontal areas. The plasticity of the nervoussystem may lead to rewiring or rerouting ofinformation acquired after the brain damage.Or the existence of hierarchically orderedrecall systems can be assumed, similar to themodels proposed for memory encoding afterdamage of relevant bottleneck structures.44With respect to the differential retrieval ofinformation acquired after brain damage (butnot before brain damage), the additionalrequirement is that the process of informationconsolidation implies the immediate establish-ment of a retrieval path. In the intact brain thisretrieval path would principally and primarilyinvolve the temporofrontal junction areas. Inthe brain with damage to this region an imme-diate retrieval path would be established toother, intact structures, lower in hierarchy,and less accurate and precise in retrieval.The proposal made by several authors

implicitly or explicitly that the storage of thememory content is composed according tolandmarks, may have the effect that after braindamage events which occurred before thatlandmark cannot be recalled, whereas thosestored thereafter can be.4 This view might alsobe in accordance with Wolpaw's that braindamage may disrupt the association betweenmemories due to the "missing link" (in thetemporofrontal junction area) which is neces-sary for the organised triggering (in the frontalportion) and access (in the temporal portion)to the engrams.45We are grateful to David Emmans for improvement of the lan-guage. The research of HJM is supported by the GermanResearch Council (DFG).

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3 Della Sala S, Laiacona M, Spinnler H, Trivelli C.Autobiographical recollection and frontal damage.Neuropsychologia 1993;31:823-39.

4 Hodges JR, McCarthy RA. Autobiographical amnesiaresulting from bilateral paramedian thalamic infarction.Brain 1993;116:921-40.

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Doctors' writing, and writingsThe quality of doctors' writing has long been theobject of writers' humour. I suspect that doctors, justas novelists, can suffer from writer's block although inthe case of the medical profession more perhaps fromlack of time rather than from a failure of inspiration.Which explanation applies to Ovid Vere, in Heart andscience, is not entirely clear. Thomas Mann's encyclo-pedia is one I have tried to emulate but as yet with no

success in finding a willing publisher!

Samuel J'ohnson, 1779, Lives of the English poets-DrydenIt is a rare kind of giblet porridge, made of the giblets ofa couple of young geese, stodged full of meteors, orbs,spheres, track, hideous draughts, dark characters,white forms, and radiant lights, designed not only toplease appetite, and indulge luxury; but it is also phys-ical, being an approved medicine to purge choler: for itis propounded by Morena, as a receipt to cure theirfathers of their choleric humours: and were it writtenin characters as barbarous as the words, might verywell pass for a doctor's bill.

Gustave Flaubert, 1856-7, Madam BovaryEmma looked at him and shrugged her shoulders.Why hadn't she at any rate one of those silent, earnesthusbands who work at their books all night-and end

up, by the time that rheumatism sets in at sixty, wearinga string of decorations on their ill-fitting dress-coats!She would have liked this name of Bovary, that washers, to be famous, on view at the book-shops, alwayscropping up in the papers, known all over France. ButCharles had no ambition.

Wilkie Collins, 1883, Heart and scienceHis restless hand unlocked a drawer, and took out amanuscript work on medicine of his own writing."Surely," he thought, "I may finish a chapter, before Igo to sea tomorrow?"

Thomas Mann, 1924, The magic mountainFamous European specialists, physicians, psycholo-gists, and economists will share in the composition ofthis encyclopedia of suffering, and the general editorialbureau at Lugano will act as the reservoir to collect allthe articles which shall flow into it . .. This great workwill not neglect the belletrist in so far as he deals withhuman suffering: a volume is projected which shallcontain a compilation and brief analysis of such mas-terpieces of the world's literature as come into ques-tion depicting one or other kind of conflict-for theconsolation and instruction of the suffering.

G D PERKINRegional Neurosciences Centre,

Charing Cross Hospital,Fulham Palace Road,London W6 8RF, UK

NEUROLOGY IN LITERATURE



j.com/

J Neurol N


eptember 1996. D

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