proof of semantics in amnesia
DESCRIPTION
AmnesiaTRANSCRIPT
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Neuropsychologia xxx (2004) xxxxxx
Remembering and forgetting of semantic16-year follow-up investigat
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nb,1,5ge, Dow6ege, Lon7rosurge8
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Abstract10
We report our long-term follow-up investigations of RFR, a post-encephalitic case of very grave anterograde and retrograde amnesia.We also describe the results of quantitative neuroimaging of his brain injury that showed bilateral and severe reduction in the hippocampalformation and medial temporal structures with sparing of left lateral/posterior and right posterior temporal cortex. We established that RFRhad a persistent severe anterograde and retrograde amnesia for personal and public events. His personal semantic knowledge was relativelyspared for thbecame amnRemarkablysemantic knability to acqand name facontemporarview.
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Keywords: A24
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1. Introdu1
It has lo2lateral med3tional mean4the human5Spiers, Ma6& Duchen7pathology,8
CorrespoE-mail add
(R. McCarthyE.Warrington
1 Universitypital, London
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e retrograde period. There was a modest and global reduction in RFRs vocabulary for words acquired in adulthood before heesic but there was no evidence of any retrograde gradient. His retrograde knowledge of people was also without any gradient., there had been no change in the extent of his semantic knowledge across a prolonged re-test interval indicating that the loss ofowledge was stable and likely to have arisen at the time of his initial lesion. RFR also showed evidence of a limited but significantuire new word meanings and a more restricted capacity for learning about new celebrities. While he was able to demonstrate face
miliarity for newly famous people, he was unable to provide much semantic detail. RFRs amnesia can be partially explained byy theories that allow for parallel cortical and hippocampal memory systems but is difficult to reconcile in detail with any extant
lished by Elsevier Ltd.
mnesia; Retrograde; Human memory system
ction
ng been recognised that amnesia arising from bi-ial temporal lobe lesions can provide an excep-s of investigating the various sub-components ofmemory system (Kopelman, 2002; Milner, 1972;guire, & Burgess, 2001; Squire, 1998; Warrington, 1992). In many cases of medial temporal lobethe damage has an acute and known date of onset
nding author.resses: [email protected]), [email protected] (M. Kopelman),@dementia.ion.ucl.ac.uk (E. Warrington).
Department of Psychiatry and Psychology, St. Thomass Hos-SE1 7EH, UK.
and the affected areas may be relatively circumscribed. The 9affected individual may present with a severe memory prob- 10lem but otherwise well preserved cognitive abilities. Despite 11a profound inability to maintain any ongoing memory for 12events, these amnesic people may nevertheless have signifi- 13cant islands of preserved memory function. For example, it is 14now universally accepted that their short-term or working 15memory may be entirely normal and that their linguistic and 16conceptual systems may also be intact. Such evidence has 17been interpreted as reflecting (at least partial) independence 18of the underlying memory subsystems (Kapur, 1999). 19
The investigation of medial temporal lobe amnesia has the 20potential to shed light on the theoretical distinction between 21memory for episodes or events and memory for semantic 22or conceptual information. Episodic memory functions are 23
see front matter 2004 Published by Elsevier Ltd.neuropsychologia.2004.06.024Rosaleen McCarthya,, Michael Kopelmaa Department of Experimental Psychology, University of Cambrid
b Institute of Psychiatry, Kings Collc Dementia Research Group, National Hospital for Neurology and Neu
Received 19 January 2004; received in revised form 14U
knowledge in amnesia: aion of RFR
Elizabeth Warringtonc
ning Street, Cambridge CB2 3EB, UKdon, UKry, Queen Square, London WC1N 3BG, UK004; accepted 29 June 2004
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2 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
severely compromised, both quantitatively and qualitatively24in amnesia, but vocabulary and semantic knowledge may25be relatively spared (Warrington, 1979). This dissociation26is mirrored27knowledge28cal dement29Cappelletti30Snowden, L31The eviden32these two c33between ep341999). The35observed i36pus wherea37with dysfun38perirhinal t39& Rossor,40
Althoug41of memory42cal and fun43and semant44memory sy45e.g. Graham46Snowden,47Are the epi48with separa49Does one s502001)? Do51activity in o52& Moscov53Does an ep54preservatio55ogy (Cerm56
There h57of episodic58semantic lo59& Hodges,601997). The61and autobio62(albeit that63not appear64the questio65spective by66a case of ch67determinin68semantic k69a case of se70Do such am71
1.1. Do am72
The pre73clinical dia741979; War75about the m76edge over77
morbid vocabulary at a consistent level or is there gradual 78forgetting of this information in the absence of continued in- 79put from the episodic memory system? One published case 80
long-term follow-up (HM) has recently been reported as 81ing mild to moderate weakness on tests sensitive to se- 82ic memory impairment H.M.s scores were borderline 83ost of the tests and were unequivocably (sic) impaired 84of the 11 tests that he performed (Schmolck, Kensinger, 85in, & Ssia haon tes
ever, iight bamne
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Can a
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2001)e hav, a casalitisarthy
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by the selective loss of vocabulary and semanticwith spared episodic memory in some of the fo-
ias (Hodges & McCarthy, 1995; Moss, Kopelman,, De Mornay Davies, & Jaldow, 2003; Talbot,loyd, Neary, & Testa, 1995; Warrington, 1975).ce for differing principal sites of pathology inlasses of disorder further bolsters the distinctionisodic and semantic memory (Mummery et al.,medial temporal amnesic syndrome is typically
n cases with bilateral lesions to the hippocam-s disorders of semantic memory are associatedction in the antero-lateral, inferior, entorhinal and
emporal cortex especially on the left (Chan, Fox,2002; Chan et al., 2001; Galton et al., 2001).h the broad distinction between these two classesdeficit seems securely established at the anatomi-ctional levels, the relative magnitudes of episodicic impairments, and the way in which the putativestems inter-relate and interact is problematic (see
& Hodges, 1997; Graham, Patterson, et al., 1999;Griffiths, et al., 1995; Snowden & Neary, 2002).sodic and semantic systems entirely independentte rules of learning and retention (Tulving, 1987)?ystem provide the gateway to the other (Tulving,they have a mutually supportive relationship withne system influencing activity in the other (Nadel
itch, 1997; Schacter, Verfaellie, & Anes, 1997)?isodic to semantic transfer result in the relativen of remote memories in medial temporal pathol-ak & OConnor, 1983)?ave been a number of studies examining the status
and autobiographical event memory in cases ofss (Coughlan & Warrington, 1981; Graham, Pratt,1998; Moss et al., 2003; Rusconi, Zago, & Basso,re is evidence for substantial sparing of episodicgraphical event knowledge in semantic dementiaperformance on standard tests of memory does
to be entirely normal). In this report, we approachn of the relationship from a complementary per-investigating the status of semantic knowledge inronic amnesia. Specifically, we were interested ing whether there was evidence for deterioration ofnowledge or acquisition of semantic knowledge invere and chronic medial temporal lobe amnesia:nesics forget, and can they remember?
nesic patients forget?
servation of basic vocabulary skills is one of thegnostic criteria for pure amnesia (Warrington,
rington & Weiskrantz, 1968), but little is knownaintenance of vocabulary and semantic knowl-
the longer term. Do amnesics retain their pre-
withshowmanton m
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quire, 2002). Other cases of medial temporal lobe 86ve been reported to show varying levels of impair- 87ts of semantic processing (Reed & Squire, 1998). 88t is unclear whether these deficits are progressive 89e predicted if they were a direct consequence of 90sic) or whether they are static and can be attributed 91al cortical pathology. While there are pointers to 92t the severity of semantic loss in amnesia is as- 93ith the magnitude of extra-hippocampal cortical 94chmolck et al., 2002), there are no longitudinal 95permit a distinction between the progressive and 96
theses. 97
mnesics remember? 98
gard to the acquisition of semantic information, 99(infantile and childhood) hippocampal pathology 100ompanying episodic memory deficit does not ap- 101lish the ability to acquire school knowledge or 102age-appropriate vocabulary (Vargha-Khadem et 103
Adult-onset cases seem to be more heterogeneous 104s of their underlying pathology and in terms of the 105
their amnesia. Some cases of adult-onset amnesia 106y impaired on antergrade tests of new vocabulary 107recognition as well as on more traditional mea- 108oratory learning (e.g. case HM (Gabrieli, Cohen, 1091988), case KJ (Wilson & Baddeley, 1988), case 110el-Clower et al., 1996), and case SS (Verfaellie, 111oth, 1995)). However, there are at least two peo- 112vere bilateral hippocampal pathology for whom 113dence of at least some sparing of anterograde new 114erson recognition abilities: case RS (Kitchener, 115McCarthy, 1998), and case PS (Verfaellie, Koseff, 116er, 2000).1 There are also two cases with sparing 117ity judgments for new famous names in the ab- 118y detailed recall or recognition capacities: case VC 119t al., 2001) and case KC (Westmacott & Moscov- 120. 121e recently conducted follow-up investigations of 122e of global amnesia due to herpes simplex en- 123
who was originally investigated in 19861988 124& Warrington, 1992; Warrington & McCarthy, 125
ase of amnesia with a very severe memory loss due to a uni-ippocampal) lesion was reported as showing normal abilitiesrade new word definition task (Van der Linden et al., 2001).right medial temporal lobe and hippocampus were spared ining direct comparisons difficult.
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R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx 3
1988). RFR had (and has) an extremely severe anterograde126and retrograde amnesia. In our previous reports, we estab-127lished that RFR had some sparing of retrograde semantic128information129retrograde130semantic k131(McCarthy132plicit retro133judgments134completion135
The pres136opportunity137semantic in138we have no139
2. Case re140
RFR wa141who becam142tack of her143from the ac144findings of145nesic syndr146evidence of147bilateral at148There was149lateral regi150lateral temp151
Table 1152measured a153(Colcheste154bilateral an155ral lobe atro156pocampal g157right, but n158termined b159the whole160significantl161panel) uses162fied MRI m163and shape i164tive to a con165of the hipp166Fig. 2 (low167hippocamp168pocampal c169pared with170
RFR wa171in August 1172in 1993 and1732000 and 2174assessment175
RFRs in176ble at an ab177tests consi178
. MRI Scan of RFR at the level of the temporal lobes. MRI scanng extensive bilateral damage to the medial temporal lobes togethernvolvement of the anterior and lateral portion of the right temporal(left hemisphere is shown on the right of this figure).
By contrast, he has consistently been severely and sig- 179ntly impaired on clinical tests of learning and memory 180
ng below 50 on the Wechsler memory scale-revised and 181n the range of chance on the Warrington RMT tests. 182
Autobiographical memory 183
FRs autobiographical recall gravely impaired. The few 184s of personal information that he can produce are very 185otyped in content and typically lack any elaborative in- 186ation or contextual detail. During the course of an in- 187w he will often spontaneously and repeatedly mention 188ippet of personal information (e.g. I had a very high 189T rating you know, delayed retention and something else 190sically a good memory. They told me my rating was very 191). When questioned about these snippets he is invariably 192
le to elaborate. Such snippets are sometimes reproduced 193tim multiple times in the course of any single testing 194
on. Our clinical notes record that similar stories were re- 195in 1986, 2002 and 2004! In a task presented both in 1986 196002 RFR was asked to write an account of his autobi- 197hy using three headings: schooldays, time in services, 198t past. His responses are shown in Table 3. 199CO
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that had been acquired during a period of dense(episodic) amnesia. He also demonstrated sparednowledge of people from the retrograde period& Warrington, 1992) and showed a range of im-grade memory abilities with preserved familiarityfor faces and names and sparing of famous name.ent long-term follow-up investigation gave us theto evaluate RFRs ability to retain and acquire
formation across a 17-year interval. In addition,w been able to obtain MRI studies of his pathology.
port
s a senior police officer (date of birth 15/03/1932)e densely amnesic in July 1985 following an at-
pes simplex encephalitis. When he had recoveredute phase of the illness there were no neurologicalnote with the exception of a severe and global am-ome. CT and subsequent MRI scanning showedbilateral medial temporal lesions and very severe
rophy of the hippocampal complex (see Fig. 1).also extensive damage throughout the anterior andons of the right temporal lobe. The left antero-oral cortex was relatively spared (Fig. 1).
shows quantified regional brain volumes for RFRccording to criteria described in detail elsewhere
r et al., 2001; Kopelman et al., 2003). RFR showedd severe (>4 S.D. below controls) medial tempo-phy, involving the hippocampus and the parahip-yri on either side. It can also be seen that RFRsot left, antero-lateral temporal lobe volume (de-y subtracting the medial temporal volume fromtemporal lobe volume in either hemisphere) was
y less than the mean of the controls. Fig. 2 (uppera 3D surface-rendered projection of these quanti-easurements to show the bilateral loss of volume
n RFRs hippocampus (upper right quadrant) rela-trol (upper left quadrant), The head, body, and tail
ocampus is evident in the control but not in RFR.er panel) shows the atrophy in RFRs combinedal formation, entorhinal, perirhinal, and parahip-ortices on either side (lower right quadrant) com-a healthy control (lower left quadrant).s initially seen for neuropsychological assessment985 and December 1986 (NHQS), subsequently1996 (St. Thomass) and most recently between
004 at his residence. The main findings from theses are summarised in Table 2.tellectual functioning has remained relatively sta-
ove average level since 1985/1986. He also passeddered sensitive to frontal lobe dysfunction with
Fig. 1showiwith icortex
ease.
nificascoriwithi
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4 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
Table 1MRI regional brain volumes in RFR and healthy subjects (methods andcontrols described in Colchester et al., 2001)
RFR Controls: mn S.D. SigIntra-cranial volume 1.31 (L) 1.33 (L) 0.12 Whole brain 0.95 (L) 1.14 (L) 0.13 Left frontal 205.7 (cm3) 250.2 (cm3) 39.1 Right frontal 200.5 (cm3) 249.0 (cm3) 36.8 Total frontal 406.2 (cm3) 499.2 (cm3) 75.3 Left temporal 71.0 (cm3) 83.9 (cm3) 11.0 Right temporal 51.0 (cm3) 91.3 (cm3) 12.6 **Total temporal 122.0 (cm3) 175.2 (cm3) 21.6 *Left antero-lat temp 69.3 (cm3) 76.9 (cm3) 11.2 Right antero-lat temp 48.5 (cm3) 84.0 (cm3) 12.9 *Total antero-lat temp 117.7 (cm3) 160.9 (cm3) 22.1 (*)Left med temp 1741 (mm3) 7044 (mm3) 731 ***Right med temp 2516 (mm3) 7280 (mm3) 820 ***Total med temp 4257 (mm3) 14324 (mm3) 1503 ***Left parahippocampal 543 (mm3) 3402 (mm3) 548 ***Right parahippocampal 854 (mm3) 3150 (mm3) 497 ***Total parahipp
Left hippocamRight hippocaTotal hippocaBelow contro(*)RFR 2 S
We wer200event me201RFR told u202thirties an203his athletic204and was a c205the dieticia206and potato207frequently208at his creat209
In respo210graphical m211Baddeley,212
Table 2Summary of n
Test
WAISWAIS-RRMT wordsRMT facesWMS genWMS delayedAttention/conVerbal fluency
MWCST
Cognitive estiInformation thdifferences be
. Surface rendered projections of hippocampus and medial temporalig. 2 shows 3D surface-rendered projections from quantified structuralof the hippocampoi in a healthy subject (upper left quadrant) and in
upper right quadrant). The head, body, and tail of the left hippocampusseen in the healthy control subject, and RFRs hippocampoi show se-ss of volume and shape. The figure also shows a 3D surface-renderedtion of the combined hippocampoi and parahippocampal gyri (includ-torhinal, perirhinal, and parahippocampal cortices) in a healthy subjectP
ocampal 1397 (mm3) 6553 (mm3) 960 ***pal 1198 (mm3) (6.5) 3642 (mm3) 372 ***mpal 1662 (mm3) (3.6) 4130 (mm3) 680 ***mpal 2860 (mm3) (4.87) 7772 (mm3) 1008 ***l mean: ***RFR > 4 S.D.; **RFR > 3 S.D.; *RFR > 2 S.D.;.D.
e only able to elicit one or two possible personalmories over the course of multiple interviews.s of a medical when he was in his early to midd had been told to go on a diet in order to maintainfitness. I was over a stone heavier than a year agoandidate for a heart attack. I saw the Doctor and
n and was told, Dont be a SAPsugar, alcohol
Fig. 2lobe. FMRIsRFR (can bevere loprojecing enUNCO
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emory interview (AMI) (Kopelman, Wilson, &1989), RFR gave just one satisfactory response
europsychological test scores
1985/1988 1993
Verbal 128*, performance 110Verbal 116, p
31/50; 27/5032/50; 26/50
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Table 3Written recall of named life periods
1986 2001
Schooldays SchooldaysAttended elementary school until the age of eleven when I entered gram-
mar school where I remained until I was sixteen or seventeen. I leftafter matriculating etc
Attended junior school in Finchley until the age of eleven followed bycollege (specializing in studying languages) to the age of seventeen
Time in services Time in servicesI served with the RAF as a photographic intelligence officer working
mainly in the middle eastRegular serviceman in the RAF for a few years (mainly spent in Egypt)
Career in police Career with policeI joined the police service in 1954 Joined the metropolitan police in 1954 stationed at Barnet for twelve years
and then at Scotland Yard until retirementRFRs written recall of his autobiography as cued by specific headings. His recall when tested in 1986 is juxtaposed with his recall in 2001.
across two occasions of testing, reporting that, when213he was working at the Institute of British Photographers in214his early 20s, there was an episode in which someone had an215accident with photographic fixer, became cross, and threw it216around. The fixer sprayed all over RFR, including his eyes,217and he had to go to the doctor. Again, this was an anecdote218he has given on several occasions.219
RFRs results on the autobiographical memory interview220(AMI) are shown in Fig. 3. RFRs scores were clearly abnor-221mal on both scales and indicative of severe retrograde and222anterograde autobiographical memory impairments. It is of223note that RFR shows significant deficits at every time pe-224riod that was tested and that he does not show any gradient225
Fig. 3. Scoresview for RFRical incidentspersonal sema
to his retroor of factsperformancbiographic(1988). Altmantic factthese itemsready been
We alsothat has beecontext indtext dependcal and pubtion questioulations, thitems suchaddress (kficult items
cts sut? WBarb
reliabnses (of celCase
confab, in prin the
FRs sas wiendenCTED
PsubjecidenDallatrolsrespokindswer.
dentet al.given
RHe windepUNCO
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on the AMI. Results on the autobiographical memory inter-and controls. The upper panel shows scores on autobiograph-(episodic information) and the lower panel shows scores forntic facts.
the difficul
Table 4MACQ resultQuestion type
Easy (N = 32)Difficult (N =Scores by RFmation at twoparentheses.OOF
grade knowledge of autobiographical incidents 226. These findings are entirely consistent with his 227e on a range tests administered to assess his auto- 228
al memory reported by McCarthy and Warrington 229hough RFRs scores on the recent personal se- 230s items of the interview were particularly weak, 231reflect anterograde memory because he had al- 232
amnesic for 10 years at the time of this testing. 233administered a newly developed questionnaire 234
n designed specifically to compare knowledge of 235ependent (generalised, mostly semantic) and con- 236ent (ephemeral, mostly episodic) autobiographi- 237lic information (the metamemory and confabula- 238nnaire (MACQ)). In an attempt to elicit confab- 239
e 64 questions were further subdivided into easy 240as Who is the Prime Minister or What is your 241nown by the majority of control subjects) and dif- 242that cannot be answered by the majority of control 243ch as Who were the boys in the Jamie Bulger in- 244
hat is your National Insurance Number? (after 245a, Cappelletti, Signorini, & Denes, 1997). Con- 246ly produce dont know, or qualified/inferential 247e.g. since it was my birthday I probably had some 248ebration) to difficult items that they cannot an- 249s of metamemory impairment may produce confi- 250ulations in response to these questions (McCarthy 251eparation). Example items from the MACQ are 252Appendix. 253
cores on the MACQ are summarised in Table 4. 254thin the range of normal controls on the context- 255t questions and even scored above the mean on 256NSY 1861 117
t items. He was given credit for knowing about 257
s
Context independent Context dependent
Personal Public Personal Public
7 (7.9) 7 (7.5) 1 (7.4) 1 (7.4)32) 5 (4.4) 4 (0.9) 0 (1.2) 0 (1.8)R and controls on the MACQ for personal and public infor-
levels of difficulty. Control scores (N = 15) are shown in
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Kennedys death and acknowledging that he had seen the258examiner at some time in the past on the context-dependent259episodic questionsbut he failed on all of the other items. For260example, he could not recall whether he had eaten breakfast,261could not name any individual who he had spoken with that262day nor co263events. Th264difficult q265know or co266
2.2. Public267
RFRs k268recall and269of famous2701999). On271scoring onl272with mean273than 2 S.D274five-choice275within 2 S.276stantially b2771980s (the278
RFRs r279questionna280cluding tho281intact subje282lands? W283pened at the28411th? Wh285minimal ep286knew that A287also that Ti288that had be289did not kno290as What c291happened a292elicit any re293when show294one of the295event look296with educa297a mean sco298
2.3. Vocab299
Relative300cabulary in301cision in th302Firstly, the303secondly, t304ciently bro305
2 Informatamnesia.
Most previous studies of retrograde (i.e. pre-morbid) vo- 306cabulary in people with severe amnesia have used a cross- 307sectional design, comparing patients semantic knowledge at 308one point ingiven amb
controce ofsia).
of damas thehave
ortexic promantichangangesa one
logy.vestigally rebularyemoryationsat wh
ory. Tcabulhasia
, 1994hoodkely to
ones
bon-Rn of v
tive toith theon ofulthooded re
xperim
arringwas a
ad enonse
gradesame
Metho
our fiarthy
itemd theng toCO
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uld he give any information about salient newsere was no tendency for him to confabulate onuestions. RFR simply responded that he did notuld not remember the relevant information.
events
nowledge of public events was investigated usingrecognition versions of a test involving picturesnews events (Kopelman, Stanhope, & Kingsley,the recall version, RFR was severely impaired,y 2025% correct across each decade, compareds of 6179% in healthy subjects. RFR was more. below the control mean for each decade. On arecognition version of this test, RFRs scores wereD. of controls for the 1960s and 1970s, but sub-elow the control mean (20% versus 91%) for theperiod during which he became ill).ecall of public episodes was also tested using aire probing 38 major events of the past 22 years (in-se that have a flashbulb status for neurologicallycts). For example What happened in the Falk-hat happened at Tiananmen Square; What hap-World Trade Building in New York on September
at happened at Bhopal? RFR could only recallisodic information about 2 of the 38 items. Hergentina had annexed the Falkland Islands2 and
ananmen square was associated with an uprisingen quelled by the government at the time but hew that this had happened in China. Questions suchan you tell me about Princess Diana, and Whatt the World Trade Building in New York did notlevant information. Indeed, he was quite puzzledn a picture of the Twin Towers being struck byhijacked planes and merely commented that theed nasty. Three control subjects (mean age 66)tional backgrounds comparable to RFR obtainedre of 32/38 correct.
ulary
ly little is known or agreed about changes to vo-medial temporal lobe amnesia. The lack of pre-
e literature can be ascribed to two main sources.experimental design has lacked sensitivity and
he range of vocabulary items has been insuffi-ad.
ion that he had re-learned since our first investigation of his
thanquenamne
sulttimenesianal cmanton se
siveno chflectpatho
Intypicvoca
tic mlimitstagemem
on vo
on apEllischildare licomm
Lamtentiosensi
Wtigatiin adexten
3. E
WRFRthat hto theretrothese
3.1.
InMcCof 50tendecordiUNOF
NSY 1861 117
time with a group of controls. This approach has 309iguous results. When patients perform less well 310ls their deficit may be interpreted as a conse- 311
their amnesia (and the lesions giving rise to this 312However, it could just as easily be a direct re- 313
age to cortical systems that arose at the same 314amnesia. Most cases of medial temporal am- 315
associated injury to the entorhinal and perirhi- 316areas that are known to be important for se- 317
cessing. If being amnesic has a persisting effect 318c representations then we might expect progres- 319eforgettingover time. However, it there are 320over time then any deficit in vocabulary might re- 321off loss of competencepossibly due to cortical 322
323
ations of retrograde semantic knowledge have also 324lied on words that were acquired in childhood (e.g. 325subscales from IQ tests; Hodges et al.s seman- 326battery). These measures have some important 327
. Most crucially, they confound the developmental 328ich the memory was acquired with the age of the 329he beneficial effects of an early age of acquisition 330ary robustness are well recognised in the literature 331and semantic memory impairment (e.g. Hirsh & 332
; Hodgson & Ellis, 1998). Words acquired early in 333are more robust to the effects of brain injury, they 334
be well established and they are also amongst the 335t in the language (Ellis & Morrison, 1998; Ellis & 336alph, 2000). If amnesia affects the long-term re- 337ocabulary then such items are going to be the least 338change. 339se considerations in mind, we conducted an inves- 340words that RFR would have initially encountered 341d and tested his knowledge for these items across 342tention intervals. 343
ent 1: vocabulary 344
ton and McCarthy (1988) previously showed that 345ble to provide definitions for a number of words 346tered the English vocabulary in the 20 years prior 347t of his illness, a period for which he had a dense 348amnesia. We were now able to investigate whether 349words had been retained. 350
d 351
rst experiment we re-administered Warrington and 352s original retrograde vocabulary test consisting 353s (Warrington & McCarthy, 1988). We also ex- 354procedure to include a further 16 items that ac- 355the Oxford dictionary of new words had entered 356
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Table 5Results of vocabulary test
Testing sessio
Pre-morbid nePost-morbid (
British Eng357nic cleansin358he was aske359the 1985 an360scored inde361a three-poin362of the defin363
3.2. Result364
RFRs s365cific (e.g. p366cessing, co367cleansing 368of ethnic m369formation370communica371tween the3722002 data373taking the m374
RFRs s375pressed as a376in Table 5.377there was378that RFR w379obtained be380(P = 0.5). T381ilar on the382specific vo383initions. H384was somew385
lary but he386had clearly387
3.3. Comm388
RFRs v389has remain390was no evi391lary that wa392amnesia ma393plausible in394terograde)395before he b396to determin397tic learning398current situ399
Table 6Example items from the new word recognition test
PartisanA machThe propictureA gamefully or
bagA smallPlasticA bag intake it hA smalla drow
xperim
FRs prelatiof amellie eon bettestedition a
nesicelliess a 30vely d.g. ha
Metho
e defi). Thie et alMiekelary innted iency (eforein the
ation wessions were transcribed and then independently scored 424three-point scale by two of the experimenters (MK and 425. The very few disagreements between their scores were 426ved by averaging. A four-choice recognition test was 427nistered immediately after the (recall) definition task. 428ple items from this test are shown in Table 6. 429
Results 430RREC
TED
P
n 1985 2002
w words (N = 50) (19651985) 85% 84%recent) new words (N = 16) (19862000) N/A 47%
lish usage since 1990 (e.g. road-rage, laptop, eth-g). The target words were read aloud to RFR andd to explain their meaning. His responses for bothd 2002 testing sessions were transcribed and werependently by two of the authors (RM and MK) ont scale reflecting the specificity and completenessition.
s
responses varied in quality from the highly spe-olaroid: camera, did away with darkroom pro-uld get the photo from the camera itself; ethnicthe practice in a couple of nations of getting ridinorities) through to more general or broad in-
(Dixons retail company; Internet to do withtions). There was a high level of agreement be-
raters on their scores for both the 1985 and thesets and the rare discrepancies were resolved by
ean of their two scores.cores for definitions given in 1985 and 2002 ex-percentage of the maximum total are summarisedIn the case of the pre-morbid retrograde words,
a very close correspondence between the wordsas able to define on the two testing occasions: hetter scores on five items and worse on five itemshe quality of his definitions was also closely sim-two occasions with considerable overlap in the
cabulary that he produced when making his def-is performance on the anterograde new wordshat less impressive than with the older vocabu-was still able to venture definitions for terms thatnot been known to him pre-morbidly.
ent
ocabulary for these pre-morbidly acquired wordsed stable across a 16-year re-test interval. Theredence that he had forgotten any of this vocabu-s first acquired in adulthood. The hypothesis thaty destabilise an established vocabulary seems im-this case. RFR scored less well on the novel (an-
vocabulary items than on those he had acquired
Fax(a)(b)(c)
(d)
Doggy(a)(b)(c)
(d)
4. E
Rto becases
Verfapariswas
definral amVerfaacros
relatiers (e
4.1.
Th2002faelliwithcabupresefrequlary bthoseeducing son a
RM)resoladmiExam
4.2.UNCO
ecame amnesic (retrograde) but it is not possiblee whether this relative weakness reflects a seman-deficit or limited exposure to new concepts in hisation.
Fig. 4 srecognitioncall tests (uthan 2 S.D.OOF
conflict within an organization or a countryine that provides information to touristscess of reproducing and transmitting printed information or
s over telephone linesin which participants are required to answer questions truth-perform some embarrassing act
stuffed toy like a bean bag that dogs like to play withbag into which a deceased dog is placedto which leftover food from a restaurant is placed in order toomeplastic tube that inflates to make a flotation device in case of
ning emergency in the water
ent 2: Verfaellie vocabulary test 400
erformance on the previous definitions task seems 401vely good when it is compared with other adult 402nesia in the literature (e.g. Kitchener et al., 1998; 403t al., 1995, 2000). In order to draw a direct com- 404ween RFR and two other published cases, RFR 405on vocabulary items that have also been used as 406nd recognition tasks with other medial tempo- 407s (i.e. PS and SS: Verfaellie et al., 1995, 2000). 408test has the advantage of sampling a vocabulary 409
-year period and also makes use of words that are 410ifficult and uncommon for British English speak- 411rd-liner; living will). 412
d 413
nition task was presented twice (in 1996 and 414s investigation used a British adaptation of Ver- 415.s (1995) task (developed by MK in collaboration 416
Verfaellie). Ten words that had entered the vo- 417each hemi-decade between 1955 and 1990 were 418
ndividually for spoken definition, as well as 12 low 419
-
8 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
Fig. 4. Recalthat entered th
riod sample435the normal436substantial437and were g438
4.3. Comm439
For the440adapted ve441ally less go442new word443can now a444
probably h445of his adult446UNCO
RREC
TED
PRO
l and recognition of new words. Percentages correct scores on recall/definition (upe language across 30 years.
d (only his data-points for the 1960s were withinrange). His recognition scores (lower panel) werely better than his recall scores on both occasions,enerally within 2 S.D.s of the controls mean.
ent
retrograde period, RFRs recall scores on thersion of Verfaellies vocabulary test were gener-od than on McCarthy and Warringtons retrogrades definition task. With Verfaellies materials, wescertain that by comparison with controls RFRas a moderate vocabulary loss that spans muchlife. While he is not clinically aphasic his vocab-
ulary is mosampled.
RFRs vpared to thamnesic foscores of 440 (retrogrfrom hers.not quite sscores of Sherpes encedifferenceseral medialeft middleOF
NSY 1861 117
per panel) and recognition (lower panel) on vocabulary items
derately blunted across all of the epochs that we 447448
ocabulary scores for 1980 and later were com- 449ose of PS (Verfaellie et al., 2000) who became 450llowing a hypoxic episode in 1981. PS obtained 4511.7 and 25%, respectively and RFRs scores of 452
ade) and 30% (anterograde) are indistinguishable 453RFRs scores for these latter two decades were 454
o severely impaired as the retrograde vocabulary 455S (Verfaellie et al., 1995), another patient with 456phalitis. This difference is possibly related to the 457in cortical extent of their lesions (SS had bilat- 458
l temporal lobe damage plus involvement of the 459and superior temporal lobe gyri whereas RFR has 460
-
RNSY 1861 117
R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx 9
relative sparing of the left temporal cortex). All three cases461show clear evidence of acquiring a limited amount of new462semantic information during the early phases of their severe463global amn464their recog465
We furt466improved p467in order to468about reco469correct in r470was eviden471responses t472ternatives i473doggy bag474for lunch b475Similarly, h476technology477by and retu478dont kno479was correc480
This value481expected o482recognition483ence betwe484task-difficu485
The resu486global amn487of memori488of the diso489Furthermor490set of item491new vocab492it is credit493restricted li494nition scor495the words496such know497and seems498Haslam, Co499
There w500retrograde501general red502at which w503to a genera504temporal lo505reduction r506English rat507
4.4. Person508
Knowle509tive and ne510can occur511
Hodges, 19512ity to recog513cases of pr514
Table 7Famous person definition
Assessment Period of peak fame
erordinordinat
erordinordinat
arthy,). In MR, it wof fri
e durinfollo
ich hiical reledgeestiga
xperimients?
e objewas a
s of peds witly shoersonossibifor pesic sy
Metho
elve002. T
d so aree des werl statuleadearthy,to provide as much information as he could in response 545individuals spoken name (Table 7). 546
Results 547
FRs responses were scored in two ways. First, he was 548credit for generating the appropriate superordinate cat- 549to which an individual belonged (e.g. politician; enter- 550
r). Secondly, the number of stimuli eliciting the super- 551CORR
ECTE
D P
esia. RFR and PS also show relative sparing ofnition, as did SS for the earliest decades.her analysed those items on which RFR showederformance under recognition testing conditions
determine whether there was something specialgnition. In 12 of the 19 items where RFR wasecognition but failed to score on definition, therece of sufficient partial knowledge in his definitiono support accurate differentiation between the al-n the recognition test (for example, he knew that areferred to food defining it as a slang expressionag, a meala snack when camping or on a trek).e knew that fax had something to do with newand information (he defined it as data returnedrnable from a computer). If we consider the 24w responses that he gave on definition task, het on seven of the relevant recognition test items.is no better than the 6 (4) correct that would ben the basis of guesswork alone (in a four-choice
test). This leads us to speculate that the differ-en RFRs recall and recognition simply reflectslty (aided by guesswork).lts of these experiments indicate that a persistingesia does not necessarily affect the maintenance
es for words that were learned prior to the onsetrder. RFR shows a stable retrograde vocabulary.e, we have converging evidence from a different
s showing that RFR is capable of acquiring someulary. His new word learning is not normal butable in view of his dense amnesia and his veryfestyle. The difference between recall and recog-es reflects RFRs partial knowledge of many ofthat he cannot define adequately. Preservation ofledge in amnesia has been documented elsewhereto characterise borderline vocabulary items (e.g.ltheart, & Cook, 1997).
as no evidence of any temporal gradient in RFRsknowledge. Rather, he seemed to have a modestuction in his vocabulary irrespective of the dateords entered the vocabulary. This could be duel loss of semantic efficacy resulting from a largebe lesion. Alternatively, it is possible that this
eflects the later adoption of some words by Britishher than North American English speakers.
knowledge
dge about people appears to have a special cogni-uro-anatomical status. Loss of person knowledgeas a highly specific semantic deficit (Greene &96; Kitchener & Hodges, 1999). Loss of the abil-nise people has been extensively documented inosopagnosia (Gainotti, Barbier, & Marra, 2003;
1988SupSub
2002SupSub
McC1993of RFedgenenc
In theto whpractknowof inv
5. Egrad
Ththerename
perioviousand pthe pedgeamne
5.1.
Twand 2lecteof thalitietionathreeMcCaskedto an
5.2.
RgivenegorytaineUNOOF
1960s 1970s 1980s
ate 8/12 8/12 11/12e detail 4 6 6
ate 8/12 9/12 9/12e detail 4 4 6
Evans, & Hodges, 1996; McNeil & Warrington, 515cCarthy and Warringtons previous investigations 516as shown that he had relatively preserved knowl- 517
ends and public figures who had risen to promi- 518g his adult life (McCarthy & Warrington, 1992). 519
wing experiments, we sought to explore the extent 520s knowledge of public figures had been spared (for 521asons, it was not possible to probe RFRs current 522of old friends and family during the present series 523tions). 524
ent 3: person knowledgetemporal 525526
ctive of this experiment was to determine whether 527ny temporal gradient in RFRs ability to define the 528ople who had risen to prominence at different time 529hin his retrograde amnesia. Although we have pre- 530wn that RFRs retrograde amnesia for new words 531al information was equivalent across time periods, 532lity remains that a gradient in retrograde knowl- 533ople may emerge over the course of a prolonged 534ndrome. 535
d 536
triples of famous personalities were tested in 1988 537he three individuals comprising each set were se- 538s to have achieved their peak fame within one 539cades: the 1960s, 1970s or 1980s. The person- 540e matched as far as possible for their occupa- 541s and significance (e.g. three trade union leaders, 542rs of the English Liberal Party: see Warrington & 5431988 for a fuller description). RFR was simply 544
-
RO
NSY 1861 117
10 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
ordinate plus appropriate identifying subordinate detail was552tallied. His scores for each class of response for the 1988 and5532002 assessment sessions are given in Table 5. Superordinate554information555and subord556descriptive557out any des558When his p559sessions, th56014-year ret561emerging t562he was not563unknown o564on 11 of th565testing sess566
5.3. Comm567
RFRs568changed ve569interval. He570define but571gradient.572
6. Experim573famous pe574
In this e575edge of his576set of peop577adulthood578was also ru579plored his580his ability t581
6.1. Metho582
The nam583authors, ar584with 24 nam585background586The stimuli587of similar l588The positio589to first, sec590gela Parke591Simone Ca592the famous593was simply594the experim595
6.2. Result596
RFR ha597these sets o598sessions. H599as the prev600
Table 8Names of historic and famous people: definition and familiarity
Assessment
8 showsr the nsting se
eyed sbusi
ncorpneral cer; Fave sus and
nces, RSolomist kns (Cole Afrient).nce agded re
insigntem les the tenera
rical ces. Hiunabl
Comm
FRs krved at intere knowconted spaas eve
ly half of the cases. Once again, there was no evidence 631y significant change. RFRs knowledge of established 632le is remarkably stable despite a persisting amnesia 633
xperiment 5: dening anterograde personalities 634
FR shows persisting knowledge of pre-morbid 635nalitieswhat about his knowledge of people who 636risen to prominence since he became amnesic? 637CO
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was provided accurately for 72% of the test itemsinate detail for 38%. In those cases where suchand elaborative detail was provided, it was with-cription of events associated with that individual.erformance was compared across the two testingere was no evidence of any forgetting across theention interval nor was there any evidence of anemporal gradient. At the level of individual items,entirely consistent in those who were known andn the two occasions. He obtained discrepant scorese 36 items gaining five characters on the secondion and losing six.
ent
knowledge of contemporary public figures hasry little in quantity or quality over a 14-year re-testwas not entirely consistent in the people he could
there was no evidence of any emerging temporal
ent 4: person knowledgehistorical andople
xperiment, we directly contrasted RFRs knowl-torical characters with his knowledge of anotherle who had risen to prominence during RFRs
(i.e. from the 1960s onwards). This experimentn on two occasionsin 1988 and 2002. We ex-
ability to judge whether names were familiar ando provide definitions for the same names.
d
es of 24 famous historical characters (includingtists, philosophers and inventors) were compared
es of more contemporary people from a variety ofs (e.g. film stars, politicians, writers, composers).were presented together with two distracter items
inguistic provenance for judgments of familiarity.n of the famous person was randomly allocatedond or third position within the triplets. (e.g. An-r, Mary Simpson, Jane Austen; Margot Fonteyn,lvin, Edith Stein). RFR was simply asked to pickname in the triplet. In the definition task, RFRgiven famous name in isolation and asked to tellenters what he knew.
s
d no difficulty in judging familiarity for either off people. He scored at ceiling on both assessmentis definitions were scored using the same criteriaious experiments and subdivided into those that
1988
2001
Tabletion fotwo te
conv
showthat ito getrainhe gname
instatail (pianerror
of thernm
Oexten(butthe iacros
and ghistofigurbeen
6.3.
Rpreseretesdinatmore
ity anHe wimateof anpeop
7. E
RpersohaveUNOF
Familiarity Definition
Contemporary Historic Response Contemporary Historic
24/24 24/24 Category 17/24 19/24Detail 12 9
24/24 24/24 Category 18/24 20/24Detail 13 13
RFRs scores for judgments of familiarity and spoken defini-ames of famous contemporary and historical personalities onssions.
uperordinate information (e.g. Elizabeth Taylor 601ness personality; Faraday scientist) and those 602orated detailed identifying information in addition 603ategory information (e.g. Lester Piggott jockey, 604
reud mind scientist). As is shown in Table 8, 605perordinate information for most of the target 606supplied relevant detail for about half. In a few 607FR was able to provide reasonable elaborative de- 608
on blessed with the epitome of wisdom Chopin 609own for his waltzes) but he also made some clear 610onel Ghadaffi: Leader of political group in one 611can countrieshe wanted home rule or self gov- 612
613
ain, there was no evidence of any forgetting across 614-test intervals. Indeed, his scores were marginally 615ificantly) better on the second testing session. At 616vel, his scores were not completely consistent 617wo testing sessions. He obtained identical scores 618ted almost identical definitions for 17/24 of the 619haracters and 16/24 of the more contemporary 620
s improved scores were for people whom he had 621e to define on the previous session. 622
ent 623
nowledge of historical characters is substantially 624nd has not been subject to decay across the test- 625
val. He also showed a pattern of better superor- 626ledge than detail information. Similarly, for the 627
mporary characters, he showed spared familiar- 628red superordinate-level knowledge of their roles. 629n able to venture specific information in approx- 630
-
RNSY 1861 117
R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx 11
7.1. Method638
A list of 27 people who had risen to prominence since the6391980s was640he knew ab641was collect642
7.2. Result643
RFR wa644tion for 8/645scriptions f646detail for 2647observed w648previous ex649ordinate in650When his p651used for th6522) his total653observed o654
7.3. Comm655
RFR sho656new people657information658on this task659people task660on the test661roneous su662
suggesting663amount of664
8. Experim665faces and n666
In our667could func668and name f669in the 197670within his671ton, 1992; W672iment 6 wa673been any f674over a 15-y675whether th676of familiar677the post-mo678
8.1. Metho679
Three di680were assem681
nence: Tw6821986 and 1683
Table 9Face familiarity judgments
Era (approximately)
sed: 198sed: 200
judgmters asype of t
fromer sets in Ron ofnknow
a MaiIngha
Stephel. Heithou
phs ofand aus pepositi
Result
FRs prity taly. Fus set w
Comm
is extainedisen p. Therlly gooin thnce foin of sprobn abon suffius faces and names. 715
iscussion 716
e have described our long-term follow-up of RFR, a 717nt with a very severe and persistent global amnesia. RFR 718nues to show a profound anterograde deficit in learning 719t new events and a severe retrograde amnesia for events 720CO
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P
prepared and RFR was asked to tell as much asout them in response to their spoken names. Dataed on three separate testing occasions
s
s able to provide accurate superordinate informa-27 names and made errors in superordinate de-or 3. He was only able to give accurate relevant/27. These scores are significantly worse than wasith the pre-morbid personalities tested in the twoperiments (chi-square = 6.95,P < 0.005 for super-formation; 9.2, P < 0.002 for detail information).erformance is scored on the same scale as was
e new word definition tasks (Experiments 1 andscore of 18.5% was substantially lower than wasn the tests of new word acquisition.
ent
ws impoverished acquisition of information about. While it is impressive that he has acquired anyin the context of his grave amnesia, his scorescontrast with his performance on the retrogradeand also seem to be less good than his scores
s of new word acquisition. He also produced er-perordinate categories for three of the charactersthat even these limited scores over-estimate of theinformation that he has acquired.
ent 6: familiarity judgments for famousames
earlier investigations, we established that RFRtion at the same level as controls on tests of faceamiliarity for people who had become prominent0s and early 1980s: a period that was includeddense retrograde amnesia (McCarthy & Warring-
arrington & McCarthy, 1988). Our aim in Exper-s two-fold. First, to determine whether there hadorgetting of this class of retrograde informationear test-retest interval and secondly to determine
ere was any evidence for anterograde acquisitionity for people who had become prominent duringrbid period.
d
fferent sets of 15 famous peoples names and facesbled from three time periods of peak promi-o were the original sets that had been tested in988. These celebrities time of peak promimence
AssesAssesRFRscharac
a T
datedfurth1990versitwo uGoldJoanKenmodeals (wtograance
famothird
8.2.
Rmiliavious1990
8.3.
Thmainhad rnesiaequateredevidedomasome
matiomatiofamo
9. D
WpatiecontiabouUNOOF
19701980 19801985 1990s onwards
Facesa Namesa Facesa Namesa Facesa Namesa
6/1988 12/15 14/15 13/15 15/15 N/A N/A1/2002 13/15 14/15 14/15 13/15 12/15 14/15ents of familiarity for the faces and names of contemporaryassessed in 1986 and 1988 and in 2001/2002.est.
approximately 19601970 and 19701985. One 684used characters who had become prominent in the 685FRs anterograde amnesic period). In the verbal 686the task, each famous name was combined with 687
n but linguistically similar distracter items (e.g. 688er, Ruth Abraham, Eva Rubens; Shirley Williams, 689m, Christine Sandys; Tony Blair, Roger Banks, 690ns). The face familiarity tests followed the same 691
ad and shoulders portraits of the same individu- 692t any salient context) were accompanied by pho- 693two unknown people (of similar general appear- 694
ge:see Fig. 5 for examples). The position of the 695rson was randomly allocated to first, second or 696on within the test triplets. 697
s 698
erformance on the retrograde face and name fa- 699sks was as competent as it had been 15 years pre- 700rthermore, his performance on the anterograde 701as at an equally satisfactory level (see Table 9). 702
ent 703
periment provides good evidence that RFR has 704his ability to judge the familiarity of people who 705
rominence during the period of his retrograde am- 706e is also evidence that his familiarity judgments are 707d for those people who must have been encoun- 708
e anterograde period. These findings extend the 709r preserved retention and acquisition beyond the 710imple general vocabulary items. Despite showing 711
lems with the acquisition of new semantic infor- 712ut newly famous people, RFR can acquire infor- 713cient to support familiarity judgments about both 714
-
O12 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
Fig. 5. Two itresidents the u
that occurr721aspect of R722temporal g723that early m724in 198519725the passage726most salien727history. Ag728concerned729extent to w730tested.731
9.1. Retrog732
There w733mantic kno734(e.g. the Ve735cially there736prolonged737tent with th738probably ar739be attribute740was no evi741ulary loss742first encoun743UNCO
RREC
TED
PRems from the anterograde famous personality familiarity test. The subject is askedpper left and lower right faces are the familiar items in these sets).
ed prior to the onset of his amnesia. A significantFRs amnesia was the absence of any reliable
radient to his impairment. There was no evidenceemories were spared when he was initially tested88 and no gradient appears to have emerged withof time. RFR has no knowledge of some of the
t episodes in his own life or in our recent culturalainst this background our investigation has beenwith exploring RFRs semantic knowledge and thehich his memory has changed since he was first
rade amnesia
as evidence of a weakness in RFRs retrograde se-wledge as compared with controls on some tasksrfaellie vocabulary test: Experiment 2), but cru-was no change in RFRs semantic knowledge overre-test/retention intervals our findings are consis-e view that the decrement in RFRs vocabularyose at the time of his initial lesion and that it cannotd to the continuing effects of his amnesia. There
dence of any consistent gradient in RFRs vocab-even when we specifically considered material
tered during the decade immediately prior to the
onset of hisRFR foundresented atpreventedAlternativeat the timebrain injurysibilities.
RFRs rilar picturelexical semedge acros4). RFR couof the nam1955 and 1details fordence of anacross the 3parable levWe found14-year re-
RFRs fprominentacross an
Isobel BarOFNSY 1861 117
to select the famous person from each array (note to non UK
amnesia. The pre-morbid (retrograde) words that 744difficult to define might have been weakly rep- 745the time of his lesion and his amnesia may have 746
them from becoming more securely established. 747ly, this vocabulary may have been well established 748of his lesion and then lost as a consequence of his 749. We are unable to distinguish between these pos- 750
751
etrograde knowledge of people showed a very sim- 752to his retrograde knowledge of other classes of 753antic information with no change in his knowl- 754
s extended retention intervals (Experiments 3 and 755ld provide broad category information about 75% 756
ed people who first rose to prominence between 757985. He was also able to provide additional salient 758over half of them. Once again, there was no evi- 759y temporal gradient in RFRs knowledge of people 7600 years that we sampled. RFR could provide com- 761els of information for named historical characters. 762that his knowledge had remained stable across a 763test interval. 764amiliarity judgments for the names and faces of 765people also showed no evidence of any change 766extended re-test interval. Personalities such as 767net, Golda Meier, Pierre Trudeau, and Russell 768
-
RR. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx 13
Harty may have faded from cultural prominence but they769were still familiar to RFR. Such findings are consistent770with the sparing of information stored in Face Recogni-771tion Units772representat773to more de774& Young,775same famil776they addre777cal syndrom778ogy (e.g.,779attribute R780tive preser781systems.782
We hav783RFRs retro784tervals. Mo785in 1988 wa786an identica787ing occasio788and recall o789ing is not c790impossible791mal or aty792bility of R793sive to us794memory. N795models) ha796pocampal i797ally rigid798working w799that such m800cay faster.801tect a sem802tion and c803cases with804issue.805
9.2. Antero806
When w807ing, we fou808ity to acqu809performanc810controls, b811edge was812trasted stro813& Moscovi814meanings i815evant in th816in the left817(Verfaellie818ter acquisit819also has si820hippocamp821would argu822
gree of semantic learning in the absence of a viable episodic 823memory. 824
RFR showed very limited anterograde semantic learning 825t peopfor onent 5)
d Bec. He
iarbhis poessive
selecf simple, wBlairomme
n quesvideseeme
cterisars toin ca
, KC isoples
RFRifferen
wordpers
s of 1mpar(Expethreeifferensure ton is peceiveable hever, iuired, his wconse
Thereiticallmansimplsubst(and pectly lople mal andmanti; Sandoscovhe fleledgeCO
RREC
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P
and Name Recognition Unitscontext freeions of personalitiesthat normally allow accesstailed episodic and semantic information (Bruce1986; Burton, Bruce, & Johnston, 1990). Theseiarity judgment tasks, and the representations thatss, are selectively impaired in other neurologi-
es arising from ventral temporal cortical pathol-McNeil & Warrington, 1991, 1993). We wouldFRs spared familiarity for people to the rela-vation of these same ventral temporal cortical
e consistently observed stability in the level ofgrade knowledge across our extended re-test in-st of the information that he knew about wordss retained in 2002. Indeed, RFR frequently usedl vocabulary for his definitions on the two test-ns! He was slightly less stable in his definitionsf famous people. Such long-term follow-up test-ommon (but see Schmolck et al., 2002) so it isto tell whether this degree of stability is a nor-pical pattern. We can only comment that the sta-FRs semantic knowledge seemed very impres-in the context of his extremely fragile episodicader and his colleagues (working with animalve recently proposed that in the absence of hip-nput, cortically-based memories may be unusu-(Nader, 2003) whereas Kali and Dayan (2004)ithin a computational framework, have suggested
emories may be acquired more slowly and de-Our data suggests that perhaps amnesia can pro-
antic store from dynamic updating, modifica-hange. Further long-term follow-up studies ofhippocampal amnesia will help to clarify this
grade amnesia
e looked at RFRs anterograde vocabulary learn-nd that he showed a limited but significant abil-ire semantic information about new words. Hise on new vocabulary tasks was less good than
ut the extent of his anterograde semantic knowl-by no means at floor. In this regard, he con-ngly with Case SS (Nadel, Samsonovich, Ryan,tch, 2000) who acquired virtually no novel wordn the post-morbid period (p. 301). It may be rel-is context that SSs lesion shows more damagelateral temporal cortex than is evident in RFRet al., 2000). RFR may also show somewhat bet-ion of new vocabulary items than case KC whognificant cortical involvement in addition to hisal lesion. (Westmacott & Moscovitch, 2001). Wee that RFR provides evidence for a limited de-
abouedgeperimDavito himfamilwithimprcouldray oexam
Tonyand cWheto proson
charaappeedgeRFRof peing.
Isple dgradegradescore
as co
30%leastthe dexponatiohas rto enHowis reqondlybe aage.be crKopeorymore
thirdis dirof petextuof se1995& Mtate tknowUNOOF
NSY 1861 117
le. He could only provide superordinate knowl- 826e-third of the names on which he was tested (Ex- 827. Culturally prominent names such as Bill Clinton, 828kham and Robin Cook were complete mysteries 829would frequently comment that the name seemed 830ut that he did not know how or why. By contrast 831or semantic knowledge of people, RFR was very 832on tests of their name and face familiarity. He 833t the famous name or famous face from an ar- 834
ilar items quickly and with little hesitation. For 835hen he was shown an array of faces including 836he immediately selected the appropriate picture 837nted I seem drawn to that one for some reason. 838tioned further about specific faces he was unable 839any information, simply commenting that the per- 840d familiar. The limited extent, and remarkable 841
tics of RFRs anterograde learning about people 842resemble the profile reported for verbal knowl- 843se KC (Westmacott & Moscovitch, 2001). Like 844able to acquire basic lexical form-representations 845namesbut these are often words without mean- 846
847
s anterograde semantic knowledge of famous peo- 848t in kind or degree from his knowledge of antero- 849s and their meanings? His scores on the antero- 850
onalities tests were certainly weak: he obtained 8518.5% for defining new people on Experiment 5 852
ed with his scores of 47% (Experiment 1) and 853riment 2) for defining new words. There are at 854possible explanations for these differences. First, 855ce might simply mirror the frequency of RFRs 856different types of knowledge. While this expla- 857
lausible, we do at least have evidence that RFR 858d sufficient exposure to many of these people 859im to judge their faces and names as familiar. 860
t remains possible that more extensive exposure 861to achieve a full semantic representation. Sec- 862eaker performance on person definition tests may 863
quence of his anterior right temporal lobe dam- 864is evidence that the right temporal cortex may 865
for knowledge of people (Kitchener et al., 1998; 866et al., 1999). However, were his person mem- 867y degraded we might also expect RFR to show 868antial retrograde loss of person knowledge. The 869ossibly strongest), possibility is that this finding 870
inked to RFRs anterograde amnesia. Knowledge 871ay have stronger links or weightings from con- 872episodic memory records than do other types 873
c knowledge (Laws, McKenna, & McCarthy, 874ers & Warrington, 1971; Viskontas, McAndrews, 875itch, 2000). Such an organisation would facili- 876xible and frequently revised semantics of person 877.
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14 R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx
9.3. Implications for theories of memory878
The characteristics of RFRs amnesia challenge the view879that the m880memory sy8811998). RFR882semantics883of any pers884dence of an885have repor886tively prese887adulthood888Squire, 200889support for890sis. Howev891to be more892ing early tim893are compa894scores). Co895had a diffe896component897component898ographical899any eviden900episodes an901implicated902memories.903
Our find904propose pa905tems. RFR906ries for epis907across his908knowledge909structural (910profile is n911sia describ912Vargha-Kh913evidence th914incremente915episodic sy916nificant pro917pocampal s918cesses (Mi919and indicat920crucial role921ries (Warrin922be required923facts.924
What ab925tific theori926cortical sys927sise that th928pal and co929the compu930McClelland931the hippoc932
guished in their speed of learning rather than in the types of 933information that they represent (McClelland, McNaughton, 934& OReilly, 1995). The hippocampal memory system learns 935
ly andory syce of
ortex tumulaultipleodic ol, 199uiredetrievgested in aorticalmantire streomou
and thmpal dgery comnd Mo
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s retrrved dan expowledgradiproblhas bgenerbut itscoverith grey thisconclntic ked butinformsia. W
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edial temporal lobes have a unified declarativestem (Squire & McKee, 1993; Squire & Zola,s retrograde knowledge of pre-morbid facts and
was very substantially better than his knowledgeonal or public events. Moreover, there was no evi-y gradient. By contrast, Stefanacci and colleaguested EP, another post-encephalitic case, who rela-rved recall of semantic facts and events from early
and childhood (Stefanacci, Buffalo, Schmolck, &0). Steffanacci et al. interpreted their findings asthe unified declarative memory system hypothe-
er, RFRs impairment in event knowledge appearsselective and more temporally extensive (involv-e-periods) than EPs (at least when the two cases
red on their autobiographical memory interviewnsequently, we would infer that RFRs lesion hasrential impact on one neurologically dissociableof the medial temporal lobe memory system: thethat is required to support memory for autobi-episodes and events. Moreover, the absence of
ce for a retrograde gradient in RFRs amnesia ford events may imply that the affected circuitry is
in the retrieval as well as in the storage of episodic
ings are more consistent with those theories thatrallel hippocampal and cortical learning subsys-s hippocampal injury has globally affected memo-odes and episodic and autobiographical incidents
life but has partially spared pre-morbid semanticand allowed a limited amount of new semantic andlexical and face familiarity) learning. While RFRsot identical to the cases of developmental amne-ed by Vargha-Khadem and colleagues (Mishkin,adem, & Gadian, 1998), he does provide furtherat semantic memory can be retained and even
d in the absence of a functioning hippocampal-stem. Taken as a whole, these findings raise sig-blems for those older theories that placed the hip-ystem at the apex of all learning and memory pro-shkin, Suzuki, Gadian, & Vargha-Khadem, 1997)e that the hippocampal system has a particularlyin the acquisition and retrieval of episodic memo-gton, 1979). This same system does not appear tofor the acquisition and retrieval of many semantic
out new learning? Current cognitive neuroscien-es of the relationship between hippocampal andtems in the acquisition of new knowledge empha-ere are normally interactions between hippocam-rtical systems in the course of new learning. Ontational consolidation framework advanced by, McNaughton, OReilly and their colleagues,
ampal and cortical systems are primarily distin-
rapidmem
absenneoc
and cM
(episNadeis reqand ris sugsentepal/cto seties aautonitchpocastroncantlcott aof KCout aprem2002
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NSY 1861 117
can re-activate or teach the slower cortical 936stem (e.g. during sleep and reminiscence). In the 937a hippocampus, it is theoretically possible for the 938o learn (albeit slowly) through repeated exposure 939tive changes in neo-cortical connection weights. 940trace theory emphasises, the type of memory 941
r semantic) rather than speed per se (Moscovitch & 9428; Nadel & Moscovitch, 1997). The hippocampus 943for episodic memories and is involved in encoding 944ing unique and specific episodes and contexts. It 945d that semantic knowledge may initially be repre- 946context-dependent manner involving hippocam- 947interactions. However, with repeated exposure 948
c information in different contexts, commonali- 949ngthened and semantic knowledge is represented 950sly at the level of neocortex. Nadel, Moscov- 951eir colleagues have argued that in cases of hip- 952amage, older semantic memories are likely to be 953
and that new semantic learning may be signifi- 954promised (Nadel & Moscovitch, 1997). Westma- 955scovitch reported exactly this profile in their study 956ely of a globally impaired episodic memory with- 957dient and sparing of remote but not very recent 958semantic memories (Westmacott & Moscovitch, 95959)). RFRs profile appears subtly different. 960nsolidation and multiple trace theories can give 961sights into the possible mechanisms whereby 962
ograde semantic knowledge has been relatively 963espite a grave amnesia. Both frameworks can also 964lanation for the relative poverty of his new seman- 965ge. However, the absence of any discernable tem- 966ent in RFRs retrograde semantic memory would 967ematic for both views. It is possible that any gra- 968een over-written by the brain injury that has 969ally compromised RFRs lexical semantic knowl- 970seems equally possible that there is no gradient to 971ed. Further cases of medial temporal lobe amne- 972ater sparing of cortical systems will undoubtedly 973issue. 974usion, we have found that RFR shows highly stable 975nowledge over a 16-year interval. He also shows 976significant learning of new semantic, lexical and 977ation in the context of very severe anterograde 978e infer that these relatively spared capacities are 979
on the left lateral and inferior temporal and bilat- 980or temporal lobe systems that have been relatively 981is pathology. 982
gement 983
to thank Prof. Narinder Kapur for his invaluable 984in facilitating this project. 985
-
RR. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx 15
Appendix A986
Example items from the MACQ test987
Context dePersonaPersonaPersona
Persona
Persona
Persona
Public k
Public k
Public k
Public u
Public u
Public uContext fre
PersonaPersonaPersona
Persona
Persona
PersonaPublic kPublic kpublic kPublic u
Public u
Public u
988
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RREC
TED
P
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you were born ?l unknown What is your mothers blood group
?l unknown What is your dentists name ?nown What country are The Pyramids in?nown What is the capital of Scotland ?nown Who is Winston Churchill?nknown What is the main diet of the Duck
Billed Platypus?nknown What is the meaning of the word
SHIBBOLETH?nknown What is the population of Kings
Lynn?
BruceJo
Burtonrec
PsCerma
retro
Chan,atr58
Chan,Lema
43Cipolo
ethip
ColchC.or
no
71Cough
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su
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Ellis,lexor
Ellis,adInch
Gabrieingres
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atrGalton
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ce
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bioHodgs
an
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roUNOOF
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Remembering and forgetting of semantic knowledge in amnesia: a 16-year follow-up investigation of RFRIntroductionDo amnesic patients forget?Can amnesics remember?
Case reportAutobiographical memoryPublic eventsVocabulary
Experiment 1: vocabularyMethodResultsComment
Experiment 2: Verfaellie vocabulary testMethodResultsCommentPerson knowledge
Experiment 3: person knowledge-temporal gradients?MethodResultsComment
Experiment 4: person knowledge-historical and famous peopleMethodResultsComment
Experiment 5: defining anterograde personalitiesMethodResultsComment
Experiment 6: familiarity judgments for famous faces and namesMethodResultsComment
DiscussionRetrograde amnesiaAnterograde amnesiaImplications for theories of memory
AcknowledgementAppendix AReferences