Download as pdf or txt
Download as pdf or txt
You are on page 1of 17

Neuropsychologia xxx (2004) xxxxxx

Remembering and forgetting of semantic knowledge in amnesia: a


16-year follow-up investigation of RFR

Rosaleen McCarthya, , Michael Kopelmanb,1 , Elizabeth Warringtonc

6
7

Department of Experimental Psychology, University of Cambridge, Downing Street, Cambridge CB2 3EB, UK
b Institute of Psychiatry, Kings College, London, UK
Dementia Research Group, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK
Received 19 January 2004; received in revised form 14 May 2004; accepted 29 June 2004

Abstract

OO
F

10

24

Keywords: Amnesia; Retrograde; Human memory system

13
14
15
16
17
18
19
20
21
22

25

3
4
5
6
7
8

It has long been recognised that amnesia arising from bilateral medial temporal lobe lesions can provide an exceptional means of investigating the various sub-components of
the human memory system (Kopelman, 2002; Milner, 1972;
Spiers, Maguire, & Burgess, 2001; Squire, 1998; Warrington
& Duchen, 1992). In many cases of medial temporal lobe
pathology, the damage has an acute and known date of onset

EC

1. Introduction

RR

TE
D

12

PR

23

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 hippocampal
formation and medial temporal structures with sparing of left lateral/posterior and right posterior temporal cortex. We established that RFR
had a persistent severe anterograde and retrograde amnesia for personal and public events. His personal semantic knowledge was relatively
spared for the retrograde period. There was a modest and global reduction in RFRs vocabulary for words acquired in adulthood before he
became amnesic but there was no evidence of any retrograde gradient. His retrograde knowledge of people was also without any gradient.
Remarkably, there had been no change in the extent of his semantic knowledge across a prolonged re-test interval indicating that the loss of
semantic knowledge was stable and likely to have arisen at the time of his initial lesion. RFR also showed evidence of a limited but significant
ability to acquire new word meanings and a more restricted capacity for learning about new celebrities. While he was able to demonstrate face
and name familiarity for newly famous people, he was unable to provide much semantic detail. RFRs amnesia can be partially explained by
contemporary theories that allow for parallel cortical and hippocampal memory systems but is difficult to reconcile in detail with any extant
view.
2004 Published by Elsevier Ltd.

11

0028-3932/$ see front matter 2004 Published by Elsevier Ltd.


doi:10.1016/j.neuropsychologia.2004.06.024

UN

1
2

CO

Corresponding author.
E-mail addresses: R.McCarthy@psychol.cam.ac.uk
(R. McCarthy), Michael.Kopelman@kcl.ac.uk (M. Kopelman),
E.Warrington@dementia.ion.ucl.ac.uk (E. Warrington).
1 University Department of Psychiatry and Psychology, St. Thomass Hospital, London SE1 7EH, UK.

and the affected areas may be relatively circumscribed. The


affected individual may present with a severe memory problem but otherwise well preserved cognitive abilities. Despite
a profound inability to maintain any ongoing memory for
events, these amnesic people may nevertheless have significant islands of preserved memory function. For example, it is
now universally accepted that their short-term or working
memory may be entirely normal and that their linguistic and
conceptual systems may also be intact. Such evidence has
been interpreted as reflecting (at least partial) independence
of the underlying memory subsystems (Kapur, 1999).
The investigation of medial temporal lobe amnesia has the
potential to shed light on the theoretical distinction between
memory for episodes or events and memory for semantic
or conceptual information. Episodic memory functions are

NSY 1861 117

9
10
11
12
13
14
15
16
17
18
19
20
21
22
23

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

72

1.1. Do amnesic patients forget?

30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70

73
74
75
76
77

TE
D

29

EC

28

RR

27

The preservation of basic vocabulary skills is one of the


clinical diagnostic criteria for pure amnesia (Warrington,
1979; Warrington & Weiskrantz, 1968), but little is known
about the maintenance of vocabulary and semantic knowledge over the longer term. Do amnesics retain their pre-

CO

26

UN

25

morbid vocabulary at a consistent level or is there gradual


forgetting of this information in the absence of continued input from the episodic memory system? One published case
with long-term follow-up (HM) has recently been reported as
showing mild to moderate weakness on tests sensitive to semantic memory impairment H.M.s scores were borderline
on most of the tests and were unequivocably (sic) impaired
on 5 of the 11 tests that he performed (Schmolck, Kensinger,
Corkin, & Squire, 2002). Other cases of medial temporal lobe
amnesia have been reported to show varying levels of impairment on tests of semantic processing (Reed & Squire, 1998).
However, it is unclear whether these deficits are progressive
(as might be predicted if they were a direct consequence of
being amnesic) or whether they are static and can be attributed
to additional cortical pathology. While there are pointers to
suggest that the severity of semantic loss in amnesia is associated with the magnitude of extra-hippocampal cortical
damage (Schmolck et al., 2002), there are no longitudinal
studies that permit a distinction between the progressive and
static hypotheses.
1.2. Can amnesics remember?

78
79
80
81
82
83
84
85
86
87
88
89
90
91
92
93
94
95
96
97

98

With regard to the acquisition of semantic information,


early-onset (infantile and childhood) hippocampal pathology
with an accompanying episodic memory deficit does not appear to abolish the ability to acquire school knowledge or
develop an age-appropriate vocabulary (Vargha-Khadem et
al., 1997). Adult-onset cases seem to be more heterogeneous
both in terms of their underlying pathology and in terms of the
severity of their amnesia. Some cases of adult-onset amnesia
are globally impaired on antergrade tests of new vocabulary
and person recognition as well as on more traditional measures of laboratory learning (e.g. case HM (Gabrieli, Cohen,
& Corkin, 1988), case KJ (Wilson & Baddeley, 1988), case
GD (Rempel-Clower et al., 1996), and case SS (Verfaellie,
Reiss, & Roth, 1995)). However, there are at least two people with severe bilateral hippocampal pathology for whom
there is evidence of at least some sparing of anterograde new
word and person recognition abilities: case RS (Kitchener,
Hodges, & McCarthy, 1998), and case PS (Verfaellie, Koseff,
& Alexander, 2000).1 There are also two cases with sparing
of familiarity judgments for new famous names in the absence of any detailed recall or recognition capacities: case VC
(Cipolotti et al., 2001) and case KC (Westmacott & Moscovitch, 2001).
We have recently conducted follow-up investigations of
RFR, a case of global amnesia due to herpes simplex encephalitis who was originally investigated in 19861988
(McCarthy & Warrington, 1992; Warrington & McCarthy,

PR

71

severely compromised, both quantitatively and qualitatively


in amnesia, but vocabulary and semantic knowledge may
be relatively spared (Warrington, 1979). This dissociation
is mirrored by the selective loss of vocabulary and semantic
knowledge with spared episodic memory in some of the focal dementias (Hodges & McCarthy, 1995; Moss, Kopelman,
Cappelletti, De Mornay Davies, & Jaldow, 2003; Talbot,
Snowden, Lloyd, Neary, & Testa, 1995; Warrington, 1975).
The evidence for differing principal sites of pathology in
these two classes of disorder further bolsters the distinction
between episodic and semantic memory (Mummery et al.,
1999). The medial temporal amnesic syndrome is typically
observed in cases with bilateral lesions to the hippocampus whereas disorders of semantic memory are associated
with dysfunction in the antero-lateral, inferior, entorhinal and
perirhinal temporal cortex especially on the left (Chan, Fox,
& Rossor, 2002; Chan et al., 2001; Galton et al., 2001).
Although the broad distinction between these two classes
of memory deficit seems securely established at the anatomical and functional levels, the relative magnitudes of episodic
and semantic impairments, and the way in which the putative
memory systems inter-relate and interact is problematic (see
e.g. Graham & Hodges, 1997; Graham, Patterson, et al., 1999;
Snowden, Griffiths, et al., 1995; Snowden & Neary, 2002).
Are the episodic and semantic systems entirely independent
with separate rules of learning and retention (Tulving, 1987)?
Does one system provide the gateway to the other (Tulving,
2001)? Do they have a mutually supportive relationship with
activity in one system influencing activity in the other (Nadel
& Moscovitch, 1997; Schacter, Verfaellie, & Anes, 1997)?
Does an episodic to semantic transfer result in the relative
preservation of remote memories in medial temporal pathology (Cermak & OConnor, 1983)?
There have been a number of studies examining the status
of episodic and autobiographical event memory in cases of
semantic loss (Coughlan & Warrington, 1981; Graham, Pratt,
& Hodges, 1998; Moss et al., 2003; Rusconi, Zago, & Basso,
1997). There is evidence for substantial sparing of episodic
and autobiographical event knowledge in semantic dementia
(albeit that performance on standard tests of memory does
not appear to be entirely normal). In this report, we approach
the question of the relationship from a complementary perspective by investigating the status of semantic knowledge in
a case of chronic amnesia. Specifically, we were interested in
determining whether there was evidence for deterioration of
semantic knowledge or acquisition of semantic knowledge in
a case of severe and chronic medial temporal lobe amnesia:
Do such amnesics forget, and can they remember?

24

OO
F

1 A third case of amnesia with a very severe memory loss due to a unilateral (left hippocampal) lesion was reported as showing normal abilities
on an anterograde new word definition task (Van der Linden et al., 2001).
However, the right medial temporal lobe and hippocampus were spared in
this case making direct comparisons difficult.

NSY 1861 117

99
100
101
102
103
104
105
106
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125

140

2. Case report

132
133
134
135
136
137
138

141
142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
159
160
161
162
163
164
165
166
167
168
169
170
171
172
173
174
175
176
177
178

RFR was a senior police officer (date of birth 15/03/1932)


who became densely amnesic in July 1985 following an attack of herpes simplex encephalitis. When he had recovered
from the acute phase of the illness there were no neurological
findings of note with the exception of a severe and global amnesic syndrome. CT and subsequent MRI scanning showed
evidence of bilateral medial temporal lesions and very severe
bilateral atrophy of the hippocampal complex (see Fig. 1).
There was also extensive damage throughout the anterior and
lateral regions of the right temporal lobe. The left anterolateral temporal cortex was relatively spared (Fig. 1).
Table 1 shows quantified regional brain volumes for RFR
measured according to criteria described in detail elsewhere
(Colchester et al., 2001; Kopelman et al., 2003). RFR showed
bilateral and severe (>4 S.D. below controls) medial temporal lobe atrophy, involving the hippocampus and the parahippocampal gyri on either side. It can also be seen that RFRs
right, but not left, antero-lateral temporal lobe volume (determined by subtracting the medial temporal volume from
the whole temporal lobe volume in either hemisphere) was
significantly less than the mean of the controls. Fig. 2 (upper
panel) uses a 3D surface-rendered projection of these quantified MRI measurements to show the bilateral loss of volume
and shape in RFRs hippocampus (upper right quadrant) relative to a control (upper left quadrant), The head, body, and tail
of the hippocampus is evident in the control but not in RFR.
Fig. 2 (lower panel) shows the atrophy in RFRs combined
hippocampal formation, entorhinal, perirhinal, and parahippocampal cortices on either side (lower right quadrant) compared with a healthy control (lower left quadrant).
RFR was initially seen for neuropsychological assessment
in August 1985 and December 1986 (NHQS), subsequently
in 1993 and 1996 (St. Thomass) and most recently between
2000 and 2004 at his residence. The main findings from these
assessments are summarised in Table 2.
RFRs intellectual functioning has remained relatively stable at an above average level since 1985/1986. He also passed
tests considered sensitive to frontal lobe dysfunction with

Fig. 1. MRI Scan of RFR at the level of the temporal lobes. MRI scan
showing extensive bilateral damage to the medial temporal lobes together
with involvement of the anterior and lateral portion of the right temporal
cortex (left hemisphere is shown on the right of this figure).

ease. By contrast, he has consistently been severely and significantly impaired on clinical tests of learning and memory
scoring below 50 on the Wechsler memory scale-revised and
within the range of chance on the Warrington RMT tests.

TE
D

131

EC

130

RR

129

CO

128

UN

127

PR

139

1988). RFR had (and has) an extremely severe anterograde


and retrograde amnesia. In our previous reports, we established that RFR had some sparing of retrograde semantic
information that had been acquired during a period of dense
retrograde (episodic) amnesia. He also demonstrated spared
semantic knowledge of people from the retrograde period
(McCarthy & Warrington, 1992) and showed a range of implicit retrograde memory abilities with preserved familiarity
judgments for faces and names and sparing of famous name
completion.
The present long-term follow-up investigation gave us the
opportunity to evaluate RFRs ability to retain and acquire
semantic information across a 17-year interval. In addition,
we have now been able to obtain MRI studies of his pathology.

126

OO
F

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

2.1. Autobiographical memory

179
180
181
182

183

RFRs autobiographical recall gravely impaired. The few


pieces of personal information that he can produce are very
stereotyped in content and typically lack any elaborative information or contextual detail. During the course of an interview he will often spontaneously and repeatedly mention
a snippet of personal information (e.g. I had a very high
DRAT rating you know, delayed retention and something else
. . . basically a good memory. They told me my rating was very
high). When questioned about these snippets he is invariably
unable to elaborate. Such snippets are sometimes reproduced
verbatim multiple times in the course of any single testing
session. Our clinical notes record that similar stories were related in 1986, 2002 and 2004! In a task presented both in 1986
and 2002 RFR was asked to write an account of his autobiography using three headings: schooldays, time in services,
recent past. His responses are shown in Table 3.
NSY 1861 117

184
185
186
187
188
189
190
191
192
193
194
195
196
197
198
199

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

RFR

Controls: mn

S.D.

Sig

Intra-cranial volume
Whole brain

1.31 (L)
0.95 (L)

1.33 (L)
1.14 (L)

0.12
0.13

Left frontal
Right frontal
Total frontal

205.7 (cm3 )
200.5 (cm3 )
406.2 (cm3 )

250.2 (cm3 )
249.0 (cm3 )
499.2 (cm3 )

39.1
36.8
75.3

Left temporal
Right temporal
Total temporal

71.0 (cm3 )
51.0 (cm3 )
122.0 (cm3 )

83.9 (cm3 )
91.3 (cm3 )
175.2 (cm3 )

11.0
12.6
21.6

**
*

Left antero-lat temp


Right antero-lat temp
Total antero-lat temp

69.3 (cm3 )
48.5 (cm3 )
117.7 (cm3 )

76.9 (cm3 )
84.0 (cm3 )
160.9 (cm3 )

11.2
12.9
22.1

*
(*)

Left med temp


Right med temp
Total med temp

1741 (mm3 )
2516 (mm3 )
4257 (mm3 )

7044 (mm3 ) 731 ***


7280 (mm3 ) 820 ***
14324 (mm3 ) 1503 ***

Left parahippocampal 543 (mm3 )


Right parahippocampal 854 (mm3 )
Total parahippocampal 1397 (mm3 )

548
497
960

3402 (mm3 )
3150 (mm3 )
6553 (mm3 )

372 ***
680 ***
1008 ***

1198 (mm3 ) (6.5) 3642 (mm3 )


1662 (mm3 ) (3.6) 4130 (mm3 )
2860 (mm3 ) (4.87) 7772 (mm3 )

Left hippocampal
Right hippocampal
Total hippocampal

***
***
***

Below control mean: ***RFR > 4 S.D.; **RFR > 3 S.D.; *RFR > 2 S.D.;
(*)RFR 2 S.D.

206
207
208
209
210
211
212

Fig. 2. Surface rendered projections of hippocampus and medial temporal


lobe. Fig. 2 shows 3D surface-rendered projections from quantified structural
MRIs of the hippocampoi in a healthy subject (upper left quadrant) and in
RFR (upper right quadrant). The head, body, and tail of the left hippocampus
can be seen in the healthy control subject, and RFRs hippocampoi show severe loss of volume and shape. The figure also shows a 3D surface-rendered
projection of the combined hippocampoi and parahippocampal gyri (including entorhinal, perirhinal, and parahippocampal cortices) in a healthy subject
(left lower panel) and in RFR (right lower panel), again showing substantial atrophy bilaterally in RFR (adapted from figure previously published in
Hippocampus (Kopelman et al., 2003).

PR

205

TE
D

204

Table 2
Summary of neuropsychological test scores

EC

203

Test

1985/1988

WAIS
WAIS-R
RMT words
RMT faces
WMS gen
WMS delayed
Attention/concentration
Verbal fluency (FAS)

Verbal 128*, performance 110

MWCST
Cognitive estimates

RR

202

1993

20002004

Verbal 116, performance 119*

Verbal 124, performance 138


25/50
31/50

31/50; 27/50
32/50; 26/50

CO

201

We were only able to elicit one or two possible personal


event memories over the course of multiple interviews.
RFR told us of a medical when he was in his early to mid
thirties and had been told to go on a diet in order to maintain
his athletic fitness. I was over a stone heavier than a year ago
and was a candidate for a heart attack. I saw the Doctor and
the dietician and was told, Dont be a SAPsugar, alcohol
and potato . . . give up S, A, P so I gave up sugar! RFR will
frequently recite this tale and never fails to show amusement
at his creative approach to dieting.
In response to the incidents questions on the autobiographical memory interview (AMI) (Kopelman, Wilson, &
Baddeley, 1989), RFR gave just one satisfactory response

<50
<50
108
55
6 categories
0 perseverations
3

6 categories
0 perseverations

Information that he had re-learned since our first investigation of his amnesia. The difference between VIQ scores on the two testing sessions is attributable to
differences between the subtests that were used. In particular, RFR obtained a Digit Span scaled score of 17 in 1985: a test that was not repeated in 1993.

UN

200

OO
F

Table 1
MRI regional brain volumes in RFR and healthy subjects (methods and
controls described in Colchester et al., 2001)

NSY 1861 117

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

Table 3
Written recall of named life periods
1986

2001

Schooldays
Attended elementary school until the age of eleven when I entered grammar school where I remained until I was sixteen or seventeen. I left
after matriculating etc
Time in services
I served with the RAF as a photographic intelligence officer working
mainly in the middle east
Career in police
I joined the police service in 1954

Schooldays
Attended junior school in Finchley until the age of eleven followed by
college (specializing in studying languages) to the age of seventeen
Time in services
Regular serviceman in the RAF for a few years (mainly spent in Egypt)
Career with police
Joined the metropolitan police in 1954 stationed at Barnet for twelve years
and then at Scotland Yard until retirement

RFRs written recall of his autobiography as cued by specific headings. His recall when tested in 1986 is juxtaposed with his recall in 2001.

220
221
222
223
224
225

OO
F

219

PR

218

to his retrograde knowledge of autobiographical incidents


or of facts. These findings are entirely consistent with his
performance on a range tests administered to assess his autobiographical memory reported by McCarthy and Warrington
(1988). Although RFRs scores on the recent personal semantic facts items of the interview were particularly weak,
these items reflect anterograde memory because he had already been amnesic for 10 years at the time of this testing.
We also administered a newly developed questionnaire
that has been designed specifically to compare knowledge of
context independent (generalised, mostly semantic) and context dependent (ephemeral, mostly episodic) autobiographical and public information (the metamemory and confabulation questionnaire (MACQ)). In an attempt to elicit confabulations, the 64 questions were further subdivided into easy
items such as Who is the Prime Minister or What is your
address (known by the majority of control subjects) and difficult items that cannot be answered by the majority of control
subjects such as Who were the boys in the Jamie Bulger incident? What is your National Insurance Number? (after
Dalla Barba, Cappelletti, Signorini, & Denes, 1997). Controls reliably produce dont know, or qualified/inferential
responses (e.g. since it was my birthday I probably had some
kind of celebration) to difficult items that they cannot answer. Cases of metamemory impairment may produce confident confabulations in response to these questions (McCarthy
et al., in preparation). Example items from the MACQ are
given in the Appendix.
RFRs scores on the MACQ are summarised in Table 4.
He was within the range of normal controls on the contextindependent questions and even scored above the mean on
the difficult items. He was given credit for knowing about

TE
D

217

EC

216

RR

215

across two occasions of testing, reporting that, when


he was working at the Institute of British Photographers in
his early 20s, there was an episode in which someone had an
accident with photographic fixer, became cross, and threw it
around. The fixer sprayed all over RFR, including his eyes,
and he had to go to the doctor. Again, this was an anecdote
he has given on several occasions.
RFRs results on the autobiographical memory interview
(AMI) are shown in Fig. 3. RFRs scores were clearly abnormal on both scales and indicative of severe retrograde and
anterograde autobiographical memory impairments. It is of
note that RFR shows significant deficits at every time period that was tested and that he does not show any gradient

CO

214

Fig. 3. Scores on the AMI. Results on the autobiographical memory interview for RFR and controls. The upper panel shows scores on autobiographical incidents (episodic information) and the lower panel shows scores for
personal semantic facts.

UN

213

Table 4
MACQ results
Question type

Easy (N = 32)
Difficult (N = 32)

Context independent

Context dependent

Personal

Public

Personal

Public

7 (7.9)
5 (4.4)

7 (7.5)
4 (0.9)

1 (7.4)
0 (1.2)

1 (7.4)
0 (1.8)

Scores by RFR and controls on the MACQ for personal and public information at two levels of difficulty. Control scores (N = 15) are shown in
parentheses.

NSY 1861 117

226
227
228
229
230
231
232
233
234
235
236
237
238
239
240
241
242
243
244
245
246
247
248
249
250
251
252
253
254
255
256
257

264
265
266

267

268
269
270
271
272
273
274
275
276
277
278
279
280
281
282
283
284
285
286
287
288
289
290
291
292
293
294
295
296
297
298

299

300
301
302
303
304
305

2.2. Public events


RFRs knowledge of public events was investigated using
recall and recognition versions of a test involving pictures
of famous news events (Kopelman, Stanhope, & Kingsley,
1999). On the recall version, RFR was severely impaired,
scoring only 2025% correct across each decade, compared
with means of 6179% in healthy subjects. RFR was more
than 2 S.D. below the control mean for each decade. On a
five-choice recognition version of this test, RFRs scores were
within 2 S.D. of controls for the 1960s and 1970s, but substantially below the control mean (20% versus 91%) for the
1980s (the period during which he became ill).
RFRs recall of public episodes was also tested using a
questionnaire probing 38 major events of the past 22 years (including those that have a flashbulb status for neurologically
intact subjects). For example What happened in the Falklands? What happened at Tiananmen Square; What happened at the World Trade Building in New York on September
11th? What happened at Bhopal? RFR could only recall
minimal episodic information about 2 of the 38 items. He
knew that Argentina had annexed the Falkland Islands2 and
also that Tiananmen square was associated with an uprising
that had been quelled by the government at the time but he
did not know that this had happened in China. Questions such
as What can you tell me about Princess Diana, and What
happened at the World Trade Building in New York did not
elicit any relevant information. Indeed, he was quite puzzled
when shown a picture of the Twin Towers being struck by
one of the hijacked planes and merely commented that the
event looked nasty. Three control subjects (mean age 66)
with educational backgrounds comparable to RFR obtained
a mean score of 32/38 correct.

Most previous studies of retrograde (i.e. pre-morbid) vocabulary in people with severe amnesia have used a crosssectional design, comparing patients semantic knowledge at
one point in time with a group of controls. This approach has
given ambiguous results. When patients perform less well
than controls their deficit may be interpreted as a consequence of their amnesia (and the lesions giving rise to this
amnesia). However, it could just as easily be a direct result of damage to cortical systems that arose at the same
time as the amnesia. Most cases of medial temporal amnesia have associated injury to the entorhinal and perirhinal cortexareas that are known to be important for semantic processing. If being amnesic has a persisting effect
on semantic representations then we might expect progressive changeforgettingover time. However, it there are
no changes over time then any deficit in vocabulary might reflect a one off loss of competencepossibly due to cortical
pathology.
Investigations of retrograde semantic knowledge have also
typically relied on words that were acquired in childhood (e.g.
vocabulary subscales from IQ tests; Hodges et al.s semantic memory battery). These measures have some important
limitations. Most crucially, they confound the developmental
stage at which the memory was acquired with the age of the
memory. The beneficial effects of an early age of acquisition
on vocabulary robustness are well recognised in the literature
on aphasia and semantic memory impairment (e.g. Hirsh &
Ellis, 1994; Hodgson & Ellis, 1998). Words acquired early in
childhood are more robust to the effects of brain injury, they
are likely to be well established and they are also amongst the
commonest in the language (Ellis & Morrison, 1998; Ellis &
Lambon-Ralph, 2000). If amnesia affects the long-term retention of vocabulary then such items are going to be the least
sensitive to change.
With these considerations in mind, we conducted an investigation of words that RFR would have initially encountered
in adulthood and tested his knowledge for these items across
extended retention intervals.

PR

263

TE
D

262

EC

261

2.3. Vocabulary

RR

260

Kennedys death and acknowledging that he had seen the


examiner at some time in the past on the context-dependent
episodic questionsbut he failed on all of the other items. For
example, he could not recall whether he had eaten breakfast,
could not name any individual who he had spoken with that
day nor could he give any information about salient news
events. There was no tendency for him to confabulate on
difficult questions. RFR simply responded that he did not
know or could not remember the relevant information.

Relatively little is known or agreed about changes to vocabulary in medial temporal lobe amnesia. The lack of precision in the literature can be ascribed to two main sources.
Firstly, the experimental design has lacked sensitivity and
secondly, the range of vocabulary items has been insufficiently broad.

CO

259

Information that he had re-learned since our first investigation of his


amnesia.

UN

258

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

OO
F

3. Experiment 1: vocabulary

306
307
308
309
310
311
312
313
314
315
316
317
318
319
320
321
322
323
324
325
326
327
328
329
330
331
332
333
334
335
336
337
338
339
340
341
342
343

344

Warrington and McCarthy (1988) previously showed that


RFR was able to provide definitions for a number of words
that had entered the English vocabulary in the 20 years prior
to the onset of his illness, a period for which he had a dense
retrograde amnesia. We were now able to investigate whether
these same words had been retained.
3.1. Method

345
346
347
348
349
350

351

In our first experiment we re-administered Warrington and


McCarthys original retrograde vocabulary test consisting
of 50 items (Warrington & McCarthy, 1988). We also extended the procedure to include a further 16 items that according to the Oxford dictionary of new words had entered
NSY 1861 117

352
353
354
355
356

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx


Table 5
Results of vocabulary test

Table 6
Example items from the new word recognition test

Testing session

1985

2002

Pre-morbid new words (N = 50) (19651985)


Post-morbid (recent) new words (N = 16) (19862000)

85%
N/A

84%
47%

Fax
(a) Partisan conflict within an organization or a country
(b) A machine that provides information to tourists
(c) The process of reproducing and transmitting printed information or
pictures over telephone lines
(d) A game in which participants are required to answer questions truthfully or perform some embarrassing act

363

British English usage since 1990 (e.g. road-rage, laptop, ethnic cleansing). The target words were read aloud to RFR and
he was asked to explain their meaning. His responses for both
the 1985 and 2002 testing sessions were transcribed and were
scored independently by two of the authors (RM and MK) on
a three-point scale reflecting the specificity and completeness
of the definition.

364

3.2. Results

4. Experiment 2: Verfaellie vocabulary test

RFRs s responses varied in quality from the highly specific (e.g. polaroid: camera, did away with darkroom processing, could get the photo from the camera itself; ethnic
cleansing the practice in a couple of nations of getting rid
of ethnic minorities) through to more general or broad information (Dixons retail company; Internet to do with
communications). There was a high level of agreement between the raters on their scores for both the 1985 and the
2002 data sets and the rare discrepancies were resolved by
taking the mean of their two scores.
RFRs scores for definitions given in 1985 and 2002 expressed as a percentage of the maximum total are summarised
in Table 5. In the case of the pre-morbid retrograde words,
there was a very close correspondence between the words
that RFR was able to define on the two testing occasions: he
obtained better scores on five items and worse on five items
(P = 0.5). The quality of his definitions was also closely similar on the two occasions with considerable overlap in the
specific vocabulary that he produced when making his definitions. His performance on the anterograde new words
was somewhat less impressive than with the older vocabulary but he was still able to venture definitions for terms that
had clearly not been known to him pre-morbidly.

RFRs performance on the previous definitions task seems


to be relatively good when it is compared with other adult
cases of amnesia in the literature (e.g. Kitchener et al., 1998;
Verfaellie et al., 1995, 2000). In order to draw a direct comparison between RFR and two other published cases, RFR
was tested on vocabulary items that have also been used as
definition and recognition tasks with other medial temporal amnesics (i.e. PS and SS: Verfaellie et al., 1995, 2000).
Verfaellies test has the advantage of sampling a vocabulary
across a 30-year period and also makes use of words that are
relatively difficult and uncommon for British English speakers (e.g. hard-liner; living will).

366
367
368
369
370
371
372
373
374
375
376
377
378
379
380
381
382
383
384
385
386
387

388

389
390
391
392
393
394
395
396
397
398
399

OO
F

365

400

PR

362

Doggy bag
(a) A small stuffed toy like a bean bag that dogs like to play with
(b) Plastic bag into which a deceased dog is placed
(c) A bag into which leftover food from a restaurant is placed in order to
take it home
(d) A small plastic tube that inflates to make a flotation device in case of
a drowning emergency in the water

4.1. Method

3.3. Comment

RFRs vocabulary for these pre-morbidly acquired words


has remained stable across a 16-year re-test interval. There
was no evidence that he had forgotten any of this vocabulary that was first acquired in adulthood. The hypothesis that
amnesia may destabilise an established vocabulary seems implausible in this case. RFR scored less well on the novel (anterograde) vocabulary items than on those he had acquired
before he became amnesic (retrograde) but it is not possible
to determine whether this relative weakness reflects a semantic learning deficit or limited exposure to new concepts in his
current situation.

401
402
403
404
405
406
407
408
409
410
411
412

413

The definition task was presented twice (in 1996 and


2002). This investigation used a British adaptation of Verfaellie et al.s (1995) task (developed by MK in collaboration
with Mieke Verfaellie). Ten words that had entered the vocabulary in each hemi-decade between 1955 and 1990 were
presented individually for spoken definition, as well as 12 low
frequency (<1 per million) words that had entered the vocabulary before 1955 (only four words in this test overlapped with
those in the previous set). Five controls matched for age and
education were also tested. RFRs responses on the two testing sessions were transcribed and then independently scored
on a three-point scale by two of the experimenters (MK and
RM). The very few disagreements between their scores were
resolved by averaging. A four-choice recognition test was
administered immediately after the (recall) definition task.
Example items from this test are shown in Table 6.

TE
D

361

EC

360

RR

359

CO

358

UN

357

4.2. Results

414
415
416
417
418
419
420
421
422
423
424
425
426
427
428
429

430

Fig. 4 summarises RFRs performance on the recall and


recognition tests in 1996 (RFR1) and 2002 (RFR2). On the recall tests (upper panel) on both occasions, he scored at or more
than 2 S.D. below the controls mean at nearly every time peNSY 1861 117

431
432
433
434

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

TE
D

PR

OO
F

EC

Fig. 4. Recall and recognition of new words. Percentages correct scores on recall/definition (upper panel) and recognition (lower panel) on vocabulary items
that entered the language across 30 years.

439

4.3. Comment

440
441
442
443
444
445
446

For the retrograde period, RFRs recall scores on the


adapted version of Verfaellies vocabulary test were generally less good than on McCarthy and Warringtons retrograde
new words definition task. With Verfaellies materials, we
can now ascertain that by comparison with controls RFR
probably has a moderate vocabulary loss that spans much
of his adult life. While he is not clinically aphasic his vocab-

CO

437

UN

436

RR

438

riod sampled (only his data-points for the 1960s were within
the normal range). His recognition scores (lower panel) were
substantially better than his recall scores on both occasions,
and were generally within 2 S.D.s of the controls mean.

435

ulary is moderately blunted across all of the epochs that we


sampled.
RFRs vocabulary scores for 1980 and later were compared to those of PS (Verfaellie et al., 2000) who became
amnesic following a hypoxic episode in 1981. PS obtained
scores of 41.7 and 25%, respectively and RFRs scores of
40 (retrograde) and 30% (anterograde) are indistinguishable
from hers. RFRs scores for these latter two decades were
not quite so severely impaired as the retrograde vocabulary
scores of SS (Verfaellie et al., 1995), another patient with
herpes encephalitis. This difference is possibly related to the
differences in cortical extent of their lesions (SS had bilateral medial temporal lobe damage plus involvement of the
left middle and superior temporal lobe gyri whereas RFR has
NSY 1861 117

447
448
449
450
451
452
453
454
455
456
457
458
459
460

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

468
469
470
471
472
473
474
475
476
477
478
479
480
481
482
483
484
485
486
487
488
489
490
491
492
493
494
495
496
497
498
499
500
501
502
503
504
505
506
507

508

509
510
511
512
513
514

Period of peak fame


1960s

1970s

1980s

1988
Superordinate
Subordinate detail

8/12
4

8/12
6

11/12
6

2002
Superordinate
Subordinate detail

8/12
4

9/12
4

9/12
6

McCarthy, Evans, & Hodges, 1996; McNeil & Warrington,


1993). In McCarthy and Warringtons previous investigations
of RFR, it was shown that he had relatively preserved knowledge of friends and public figures who had risen to prominence during his adult life (McCarthy & Warrington, 1992).
In the following experiments, we sought to explore the extent
to which his knowledge of public figures had been spared (for
practical reasons, it was not possible to probe RFRs current
knowledge of old friends and family during the present series
of investigations).

OO
F

467

Assessment

5. Experiment 3: person knowledgetemporal


gradients?
The objective of this experiment was to determine whether
there was any temporal gradient in RFRs ability to define the
names of people who had risen to prominence at different time
periods within his retrograde amnesia. Although we have previously shown that RFRs retrograde amnesia for new words
and personal information was equivalent across time periods,
the possibility remains that a gradient in retrograde knowledge for people may emerge over the course of a prolonged
amnesic syndrome.

PR

466

Table 7
Famous person definition

TE
D

465

EC

464

RR

463

relative sparing of the left temporal cortex). All three cases


show clear evidence of acquiring a limited amount of new
semantic information during the early phases of their severe
global amnesia. RFR and PS also show relative sparing of
their recognition, as did SS for the earliest decades.
We further analysed those items on which RFR showed
improved performance under recognition testing conditions
in order to determine whether there was something special
about recognition. In 12 of the 19 items where RFR was
correct in recognition but failed to score on definition, there
was evidence of sufficient partial knowledge in his definition
responses to support accurate differentiation between the alternatives in the recognition test (for example, he knew that a
doggy bag referred to food defining it as a slang expression
for lunch bag, a meala snack when camping or on a trek).
Similarly, he knew that fax had something to do with new
technology and information (he defined it as data returned
by and returnable from a computer). If we consider the 24
dont know responses that he gave on definition task, he
was correct on seven of the relevant recognition test items.
This value is no better than the 6 (4) correct that would be
expected on the basis of guesswork alone (in a four-choice
recognition test). This leads us to speculate that the difference between RFRs recall and recognition simply reflects
task-difficulty (aided by guesswork).
The results of these experiments indicate that a persisting
global amnesia does not necessarily affect the maintenance
of memories for words that were learned prior to the onset
of the disorder. RFR shows a stable retrograde vocabulary.
Furthermore, we have converging evidence from a different
set of items showing that RFR is capable of acquiring some
new vocabulary. His new word learning is not normal but
it is creditable in view of his dense amnesia and his very
restricted lifestyle. The difference between recall and recognition scores reflects RFRs partial knowledge of many of
the words that he cannot define adequately. Preservation of
such knowledge in amnesia has been documented elsewhere
and seems to characterise borderline vocabulary items (e.g.
Haslam, Coltheart, & Cook, 1997).
There was no evidence of any temporal gradient in RFRs
retrograde knowledge. Rather, he seemed to have a modest
general reduction in his vocabulary irrespective of the date
at which words entered the vocabulary. This could be due
to a general loss of semantic efficacy resulting from a large
temporal lobe lesion. Alternatively, it is possible that this
reduction reflects the later adoption of some words by British
English rather than North American English speakers.
4.4. Person knowledge

Knowledge about people appears to have a special cognitive and neuro-anatomical status. Loss of person knowledge
can occur as a highly specific semantic deficit (Greene &
Hodges, 1996; Kitchener & Hodges, 1999). Loss of the ability to recognise people has been extensively documented in
cases of prosopagnosia (Gainotti, Barbier, & Marra, 2003;

CO

462

UN

461

5.1. Method

515
516
517
518
519
520
521
522
523
524

525
526

527
528
529
530
531
532
533
534
535

536

Twelve triples of famous personalities were tested in 1988


and 2002. The three individuals comprising each set were selected so as to have achieved their peak fame within one
of three decades: the 1960s, 1970s or 1980s. The personalities were matched as far as possible for their occupational status and significance (e.g. three trade union leaders,
three leaders of the English Liberal Party: see Warrington &
McCarthy, 1988 for a fuller description). RFR was simply
asked to provide as much information as he could in response
to an individuals spoken name (Table 7).
5.2. Results

537
538
539
540
541
542
543
544
545
546

547

RFRs responses were scored in two ways. First, he was


given credit for generating the appropriate superordinate category to which an individual belonged (e.g. politician; entertainer). Secondly, the number of stimuli eliciting the superNSY 1861 117

548
549
550
551

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

566

ordinate plus appropriate identifying subordinate detail was


tallied. His scores for each class of response for the 1988 and
2002 assessment sessions are given in Table 5. Superordinate
information was provided accurately for 72% of the test items
and subordinate detail for 38%. In those cases where such
descriptive and elaborative detail was provided, it was without any description of events associated with that individual.
When his performance was compared across the two testing
sessions, there was no evidence of any forgetting across the
14-year retention interval nor was there any evidence of an
emerging temporal gradient. At the level of individual items,
he was not entirely consistent in those who were known and
unknown on the two occasions. He obtained discrepant scores
on 11 of the 36 items gaining five characters on the second
testing session and losing six.

567

5.3. Comment

552
553
554
555
556
557
558
559
560
561
562
563
564
565

568
569
570
571
572

573
574

RFRs knowledge of contemporary public figures has


changed very little in quantity or quality over a 14-year re-test
interval. He was not entirely consistent in the people he could
define but there was no evidence of any emerging temporal
gradient.
6. Experiment 4: person knowledgehistorical and
famous people

582

6.1. Method

577
578
579
580

TE
D

576

596

6.2. Results

587
588
589
590
591
592
593
594

597
598
599
600

RR

586

CO

585

RFR had no difficulty in judging familiarity for either of


these sets of people. He scored at ceiling on both assessment
sessions. His definitions were scored using the same criteria
as the previous experiments and subdivided into those that

UN

584

EC

595

The names of 24 famous historical characters (including


authors, artists, philosophers and inventors) were compared
with 24 names of more contemporary people from a variety of
backgrounds (e.g. film stars, politicians, writers, composers).
The stimuli were presented together with two distracter items
of similar linguistic provenance for judgments of familiarity.
The position of the famous person was randomly allocated
to first, second or third position within the triplets. (e.g. Angela Parker, Mary Simpson, Jane Austen; Margot Fonteyn,
Simone Calvin, Edith Stein). RFR was simply asked to pick
the famous name in the triplet. In the definition task, RFR
was simply given famous name in isolation and asked to tell
the experimenters what he knew.

583

Assessment Familiarity

Definition

Contemporary Historic Response Contemporary Historic


1988

24/24

24/24

Category 17/24
Detail
12

19/24
9

2001

24/24

24/24

Category 18/24
Detail
13

20/24
13

Table 8 shows RFRs scores for judgments of familiarity and spoken definition for the names of famous contemporary and historical personalities on
two testing sessions.

conveyed superordinate information (e.g. Elizabeth Taylor


show business personality; Faraday scientist) and those
that incorporated detailed identifying information in addition
to general category information (e.g. Lester Piggott jockey,
trainer; Freud mind scientist). As is shown in Table 8,
he gave superordinate information for most of the target
names and supplied relevant detail for about half. In a few
instances, RFR was able to provide reasonable elaborative detail (Solomon blessed with the epitome of wisdom Chopin
pianist known for his waltzes) but he also made some clear
errors (Colonel Ghadaffi: Leader of political group in one
of the African countrieshe wanted home rule or self government).
Once again, there was no evidence of any forgetting across
extended re-test intervals. Indeed, his scores were marginally
(but insignificantly) better on the second testing session. At
the item level, his scores were not completely consistent
across the two testing sessions. He obtained identical scores
and generated almost identical definitions for 17/24 of the
historical characters and 16/24 of the more contemporary
figures. His improved scores were for people whom he had
been unable to define on the previous session.

PR

581

In this experiment, we directly contrasted RFRs knowledge of historical characters with his knowledge of another
set of people who had risen to prominence during RFRs
adulthood (i.e. from the 1960s onwards). This experiment
was also run on two occasionsin 1988 and 2002. We explored his ability to judge whether names were familiar and
his ability to provide definitions for the same names.

575

Table 8
Names of historic and famous people: definition and familiarity

OO
F

10

6.3. Comment

601
602
603
604
605
606
607
608
609
610
611
612
613
614
615
616
617
618
619
620
621
622

623

RFRs knowledge of historical characters is substantially


preserved and has not been subject to decay across the testretest interval. He also showed a pattern of better superordinate knowledge than detail information. Similarly, for the
more contemporary characters, he showed spared familiarity and spared superordinate-level knowledge of their roles.
He was even able to venture specific information in approximately half of the cases. Once again, there was no evidence
of any significant change. RFRs knowledge of established
people is remarkably stable despite a persisting amnesia

7. Experiment 5: dening anterograde personalities


RFR shows persisting knowledge of pre-morbid
personalitieswhat about his knowledge of people who
have risen to prominence since he became amnesic?
NSY 1861 117

624
625
626
627
628
629
630
631
632
633

634

635
636
637

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx


Table 9
Face familiarity judgments

7.1. Method

642

A list of 27 people who had risen to prominence since the


1980s was prepared and RFR was asked to tell as much as
he knew about them in response to their spoken names. Data
was collected on three separate testing occasions

643

7.2. Results

641

644
645
646
647
648
649
650
651
652
653
654

655

656
657
658
659
660
661
662
663
664

665
666

RFR was able to provide accurate superordinate information for 8/27 names and made errors in superordinate descriptions for 3. He was only able to give accurate relevant
detail for 2/27. These scores are significantly worse than was
observed with the pre-morbid personalities tested in the two
previous experiments (chi-square = 6.95, P < 0.005 for superordinate information; 9.2, P < 0.002 for detail information).
When his performance is scored on the same scale as was
used for the new word definition tasks (Experiments 1 and
2) his total score of 18.5% was substantially lower than was
observed on the tests of new word acquisition.
7.3. Comment
RFR shows impoverished acquisition of information about
new people. While it is impressive that he has acquired any
information in the context of his grave amnesia, his scores
on this task contrast with his performance on the retrograde
people task and also seem to be less good than his scores
on the tests of new word acquisition. He also produced erroneous superordinate categories for three of the characters
suggesting that even these limited scores over-estimate of the
amount of information that he has acquired.

8. Experiment 6: familiarity judgments for famous


faces and names

679

8.1. Method

672
673
674
675
676
677

680
681
682
683

RR

671

CO

670

Three different sets of 15 famous peoples names and faces


were assembled from three time periods of peak prominence: Two were the original sets that had been tested in
1986 and 1988. These celebrities time of peak promimence

UN

669

EC

678

668

19701980

19801985

1990s onwards

Facesa

Namesa

Facesa

Namesa

Facesa Namesa

14/15
14/15

13/15
14/15

15/15
13/15

N/A
12/15

Assessed: 1986/1988 12/15


Assessed: 2001/2002 13/15

In our earlier investigations, we established that RFR


could function at the same level as controls on tests of face
and name familiarity for people who had become prominent
in the 1970s and early 1980s: a period that was included
within his dense retrograde amnesia (McCarthy & Warrington, 1992; Warrington & McCarthy, 1988). Our aim in Experiment 6 was two-fold. First, to determine whether there had
been any forgetting of this class of retrograde information
over a 15-year test-retest interval and secondly to determine
whether there was any evidence for anterograde acquisition
of familiarity for people who had become prominent during
the post-morbid period.

667

Era (approximately)

N/A
14/15

RFRs judgments of familiarity for the faces and names of contemporary


characters as assessed in 1986 and 1988 and in 2001/2002.
a Type of test.

dated from approximately 19601970 and 19701985. One


further set used characters who had become prominent in the
1990s in RFRs anterograde amnesic period). In the verbal
version of the task, each famous name was combined with
two unknown but linguistically similar distracter items (e.g.
Golda Maier, Ruth Abraham, Eva Rubens; Shirley Williams,
Joan Ingham, Christine Sandys; Tony Blair, Roger Banks,
Ken Stephens). The face familiarity tests followed the same
model. Head and shoulders portraits of the same individuals (without any salient context) were accompanied by photographs of two unknown people (of similar general appearance and age:see Fig. 5 for examples). The position of the
famous person was randomly allocated to first, second or
third position within the test triplets.

OO
F

640

8.2. Results

684
685
686
687
688
689
690
691
692
693
694
695
696
697

698

RFRs performance on the retrograde face and name familiarity tasks was as competent as it had been 15 years previously. Furthermore, his performance on the anterograde
1990s set was at an equally satisfactory level (see Table 9).

TE
D

639

PR

638

11

8.3. Comment

699
700
701
702

703

This experiment provides good evidence that RFR has


maintained his ability to judge the familiarity of people who
had risen prominence during the period of his retrograde amnesia. There is also evidence that his familiarity judgments are
equally good for those people who must have been encountered in the anterograde period. These findings extend the
evidence for preserved retention and acquisition beyond the
domain of simple general vocabulary items. Despite showing
some problems with the acquisition of new semantic information about newly famous people, RFR can acquire information sufficient to support familiarity judgments about both
famous faces and names.

9. Discussion

704
705
706
707
708
709
710
711
712
713
714
715

716

We have described our long-term follow-up of RFR, a


patient with a very severe and persistent global amnesia. RFR
continues to show a profound anterograde deficit in learning
about new events and a severe retrograde amnesia for events
NSY 1861 117

717
718
719
720

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

OO
F

12

PR

Fig. 5. Two items from the anterograde famous personality familiarity test. The subject is asked to select the famous person from each array (note to non UK
residents the upper left and lower right faces are the familiar items in these sets).

732

9.1. Retrograde amnesia

726
727
728
729
730

733
734
735
736
737
738
739
740
741
742
743

EC

725

There was evidence of a weakness in RFRs retrograde semantic knowledge as compared with controls on some tasks
(e.g. the Verfaellie vocabulary test: Experiment 2), but crucially there was no change in RFRs semantic knowledge over
prolonged re-test/retention intervals our findings are consistent with the view that the decrement in RFRs vocabulary
probably arose at the time of his initial lesion and that it cannot
be attributed to the continuing effects of his amnesia. There
was no evidence of any consistent gradient in RFRs vocabulary losseven when we specifically considered material
first encountered during the decade immediately prior to the

RR

724

CO

723

UN

722

TE
D

731

that occurred prior to the onset of his amnesia. A significant


aspect of RFRs amnesia was the absence of any reliable
temporal gradient to his impairment. There was no evidence
that early memories were spared when he was initially tested
in 19851988 and no gradient appears to have emerged with
the passage of time. RFR has no knowledge of some of the
most salient episodes in his own life or in our recent cultural
history. Against this background our investigation has been
concerned with exploring RFRs semantic knowledge and the
extent to which his memory has changed since he was first
tested.

721

onset of his amnesia. The pre-morbid (retrograde) words that


RFR found difficult to define might have been weakly represented at the time of his lesion and his amnesia may have
prevented them from becoming more securely established.
Alternatively, this vocabulary may have been well established
at the time of his lesion and then lost as a consequence of his
brain injury. We are unable to distinguish between these possibilities.
RFRs retrograde knowledge of people showed a very similar picture to his retrograde knowledge of other classes of
lexical semantic information with no change in his knowledge across extended retention intervals (Experiments 3 and
4). RFR could provide broad category information about 75%
of the named people who first rose to prominence between
1955 and 1985. He was also able to provide additional salient
details for over half of them. Once again, there was no evidence of any temporal gradient in RFRs knowledge of people
across the 30 years that we sampled. RFR could provide comparable levels of information for named historical characters.
We found that his knowledge had remained stable across a
14-year re-test interval.
RFRs familiarity judgments for the names and faces of
prominent people also showed no evidence of any change
across an extended re-test interval. Personalities such as
Isobel Barnet, Golda Meier, Pierre Trudeau, and Russell
NSY 1861 117

744
745
746
747
748
749
750
751
752
753
754
755
756
757
758
759
760
761
762
763
764
765
766
767
768

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

776
777
778
779
780
781
782
783
784
785
786
787
788
789
790
791
792
793
794
795
796
797
798
799
800
801
802
803
804

807
808
809
810
811
812
813
814
815
816
817
818
819
820
821
822

When we looked at RFRs anterograde vocabulary learning, we found that he showed a limited but significant ability to acquire semantic information about new words. His
performance on new vocabulary tasks was less good than
controls, but the extent of his anterograde semantic knowledge was by no means at floor. In this regard, he contrasted strongly with Case SS (Nadel, Samsonovich, Ryan,
& Moscovitch, 2000) who acquired virtually no novel word
meanings in the post-morbid period (p. 301). It may be relevant in this context that SSs lesion shows more damage
in the left lateral temporal cortex than is evident in RFR
(Verfaellie et al., 2000). RFR may also show somewhat better acquisition of new vocabulary items than case KC who
also has significant cortical involvement in addition to his
hippocampal lesion. (Westmacott & Moscovitch, 2001). We
would argue that RFR provides evidence for a limited de-

EC

775

RR

774

CO

773

UN

772

OO
F

9.2. Anterograde amnesia

771

gree of semantic learning in the absence of a viable episodic


memory.
RFR showed very limited anterograde semantic learning
about people. He could only provide superordinate knowledge for one-third of the names on which he was tested (Experiment 5). Culturally prominent names such as Bill Clinton,
David Beckham and Robin Cook were complete mysteries
to him. He would frequently comment that the name seemed
familiarbut that he did not know how or why. By contrast
with his poor semantic knowledge of people, RFR was very
impressive on tests of their name and face familiarity. He
could select the famous name or famous face from an array of similar items quickly and with little hesitation. For
example, when he was shown an array of faces including
Tony Blair he immediately selected the appropriate picture
and commented I seem drawn to that one for some reason.
When questioned further about specific faces he was unable
to provide any information, simply commenting that the person seemed familiar. The limited extent, and remarkable
characteristics of RFRs anterograde learning about people
appears to resemble the profile reported for verbal knowledge in case KC (Westmacott & Moscovitch, 2001). Like
RFR, KC is able to acquire basic lexical form-representations
of peoples namesbut these are often words without meaning.
Is RFRs anterograde semantic knowledge of famous people different in kind or degree from his knowledge of anterograde words and their meanings? His scores on the anterograde personalities tests were certainly weak: he obtained
scores of 18.5% for defining new people on Experiment 5
as compared with his scores of 47% (Experiment 1) and
30% (Experiment 2) for defining new words. There are at
least three possible explanations for these differences. First,
the difference might simply mirror the frequency of RFRs
exposure to different types of knowledge. While this explanation is plausible, we do at least have evidence that RFR
has received sufficient exposure to many of these people
to enable him to judge their faces and names as familiar.
However, it remains possible that more extensive exposure
is required to achieve a full semantic representation. Secondly, his weaker performance on person definition tests may
be a consequence of his anterior right temporal lobe damage. There is evidence that the right temporal cortex may
be critical for knowledge of people (Kitchener et al., 1998;
Kopelman et al., 1999). However, were his person memory simply degraded we might also expect RFR to show
more substantial retrograde loss of person knowledge. The
third (and possibly strongest), possibility is that this finding
is directly linked to RFRs anterograde amnesia. Knowledge
of people may have stronger links or weightings from contextual and episodic memory records than do other types
of semantic knowledge (Laws, McKenna, & McCarthy,
1995; Sanders & Warrington, 1971; Viskontas, McAndrews,
& Moscovitch, 2000). Such an organisation would facilitate the flexible and frequently revised semantics of person
knowledge.

PR

806

770

TE
D

805

Harty may have faded from cultural prominence but they


were still familiar to RFR. Such findings are consistent
with the sparing of information stored in Face Recognition Units and Name Recognition Unitscontext free
representations of personalitiesthat normally allow access
to more detailed episodic and semantic information (Bruce
& Young, 1986; Burton, Bruce, & Johnston, 1990). These
same familiarity judgment tasks, and the representations that
they address, are selectively impaired in other neurological syndromes arising from ventral temporal cortical pathology (e.g., McNeil & Warrington, 1991, 1993). We would
attribute RFRs spared familiarity for people to the relative preservation of these same ventral temporal cortical
systems.
We have consistently observed stability in the level of
RFRs retrograde knowledge across our extended re-test intervals. Most of the information that he knew about words
in 1988 was retained in 2002. Indeed, RFR frequently used
an identical vocabulary for his definitions on the two testing occasions! He was slightly less stable in his definitions
and recall of famous people. Such long-term follow-up testing is not common (but see Schmolck et al., 2002) so it is
impossible to tell whether this degree of stability is a normal or atypical pattern. We can only comment that the stability of RFRs semantic knowledge seemed very impressive to us in the context of his extremely fragile episodic
memory. Nader and his colleagues (working with animal
models) have recently proposed that in the absence of hippocampal input, cortically-based memories may be unusually rigid (Nader, 2003) whereas Kali and Dayan (2004)
working within a computational framework, have suggested
that such memories may be acquired more slowly and decay faster. Our data suggests that perhaps amnesia can protect a semantic store from dynamic updating, modification and change. Further long-term follow-up studies of
cases with hippocampal amnesia will help to clarify this
issue.

769

13

NSY 1861 117

823
824
825
826
827
828
829
830
831
832
833
834
835
836
837
838
839
840
841
842
843
844
845
846
847
848
849
850
851
852
853
854
855
856
857
858
859
860
861
862
863
864
865
866
867
868
869
870
871
872
873
874
875
876
877

884
885
886
887
888
889
890
891
892
893
894
895
896
897
898
899
900
901
902
903
904
905
906
907
908
909
910
911
912
913
914
915
916
917
918
919
920
921
922
923
924
925
926
927
928
929
930
931
932

guished in their speed of learning rather than in the types of


information that they represent (McClelland, McNaughton,
& OReilly, 1995). The hippocampal memory system learns
rapidly and can re-activate or teach the slower cortical
memory system (e.g. during sleep and reminiscence). In the
absence of a hippocampus, it is theoretically possible for the
neocortex to learn (albeit slowly) through repeated exposure
and cumulative changes in neo-cortical connection weights.
Multiple trace theory emphasises, the type of memory
(episodic or semantic) rather than speed per se (Moscovitch &
Nadel, 1998; Nadel & Moscovitch, 1997). The hippocampus
is required for episodic memories and is involved in encoding
and retrieving unique and specific episodes and contexts. It
is suggested that semantic knowledge may initially be represented in a context-dependent manner involving hippocampal/cortical interactions. However, with repeated exposure
to semantic information in different contexts, commonalities are strengthened and semantic knowledge is represented
autonomously at the level of neocortex. Nadel, Moscovitch and their colleagues have argued that in cases of hippocampal damage, older semantic memories are likely to be
strongerand that new semantic learning may be significantly compromised (Nadel & Moscovitch, 1997). Westmacott and Moscovitch reported exactly this profile in their study
of KC namely of a globally impaired episodic memory without any gradient and sparing of remote but not very recent
premorbid semantic memories (Westmacott & Moscovitch,
2002; (p. 159)). RFRs profile appears subtly different.
Both consolidation and multiple trace theories can give
valuable insights into the possible mechanisms whereby
RFRs retrograde semantic knowledge has been relatively
preserved despite a grave amnesia. Both frameworks can also
give an explanation for the relative poverty of his new semantic knowledge. However, the absence of any discernable temporal gradient in RFRs retrograde semantic memory would
seem problematic for both views. It is possible that any gradient has been over-written by the brain injury that has
more generally compromised RFRs lexical semantic knowledge but it seems equally possible that there is no gradient to
be discovered. Further cases of medial temporal lobe amnesia with greater sparing of cortical systems will undoubtedly
clarify this issue.
In conclusion, we have found that RFR shows highly stable
semantic knowledge over a 16-year interval. He also shows
limited but significant learning of new semantic, lexical and
face information in the context of very severe anterograde
amnesia. We infer that these relatively spared capacities are
dependent on the left lateral and inferior temporal and bilateral posterior temporal lobe systems that have been relatively
spared by his pathology.

PR

883

TE
D

882

EC

881

RR

880

The characteristics of RFRs amnesia challenge the view


that the medial temporal lobes have a unified declarative
memory system (Squire & McKee, 1993; Squire & Zola,
1998). RFRs retrograde knowledge of pre-morbid facts and
semantics was very substantially better than his knowledge
of any personal or public events. Moreover, there was no evidence of any gradient. By contrast, Stefanacci and colleagues
have reported EP, another post-encephalitic case, who relatively preserved recall of semantic facts and events from early
adulthood and childhood (Stefanacci, Buffalo, Schmolck, &
Squire, 2000). Steffanacci et al. interpreted their findings as
support for the unified declarative memory system hypothesis. However, RFRs impairment in event knowledge appears
to be more selective and more temporally extensive (involving early time-periods) than EPs (at least when the two cases
are compared on their autobiographical memory interview
scores). Consequently, we would infer that RFRs lesion has
had a differential impact on one neurologically dissociable
component of the medial temporal lobe memory system: the
component that is required to support memory for autobiographical episodes and events. Moreover, the absence of
any evidence for a retrograde gradient in RFRs amnesia for
episodes and events may imply that the affected circuitry is
implicated in the retrieval as well as in the storage of episodic
memories.
Our findings are more consistent with those theories that
propose parallel hippocampal and cortical learning subsystems. RFRs hippocampal injury has globally affected memories for episodes and episodic and autobiographical incidents
across his life but has partially spared pre-morbid semantic
knowledge and allowed a limited amount of new semantic and
structural (lexical and face familiarity) learning. While RFRs
profile is not identical to the cases of developmental amnesia described by Vargha-Khadem and colleagues (Mishkin,
Vargha-Khadem, & Gadian, 1998), he does provide further
evidence that semantic memory can be retained and even
incremented in the absence of a functioning hippocampalepisodic system. Taken as a whole, these findings raise significant problems for those older theories that placed the hippocampal system at the apex of all learning and memory processes (Mishkin, Suzuki, Gadian, & Vargha-Khadem, 1997)
and indicate that the hippocampal system has a particularly
crucial role in the acquisition and retrieval of episodic memories (Warrington, 1979). This same system does not appear to
be required for the acquisition and retrieval of many semantic
facts.
What about new learning? Current cognitive neuroscientific theories of the relationship between hippocampal and
cortical systems in the acquisition of new knowledge emphasise that there are normally interactions between hippocampal and cortical systems in the course of new learning. On
the computational consolidation framework advanced by
McClelland, McNaughton, OReilly and their colleagues,
the hippocampal and cortical systems are primarily distin-

CO

879

9.3. Implications for theories of memory

UN

878

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

OO
F

14

Acknowledgement

933
934
935
936
937
938
939
940
941
942
943
944
945
946
947
948
949
950
951
952
953
954
955
956
957
958
959
960
961
962
963
964
965
966
967
968
969
970
971
972
973
974
975
976
977
978
979
980
981
982

983

We wish to thank Prof. Narinder Kapur for his invaluable


assistance in facilitating this project.
NSY 1861 117

984
985

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

References

Personal unknown
Personal unknown
Personal unknown
Public known
Public known
Public known
Public unknown

Public unknown
Context free
Personal known
Personal known
Personal known
Personal unknown
Personal unknown

CO

What is the population of Kings


Lynn?

UN

988

Are you married ?


What is your date of birth ?
What
Newspaper/brand
of
cigarettes do you use ?
How much did you weigh when
you were born ?
What is your mothers blood group
?
What is your dentists name ?
What country are The Pyramids in?
What is the capital of Scotland ?
Who is Winston Churchill?
What is the main diet of the Duck
Billed Platypus?
What is the meaning of the word
SHIBBOLETH?

RR

Personal unknown
Public known
Public known
public known
Public unknown

Public unknown

What were you doing on 15 March,


1982?
What were you doing on this day
last year?
What happened in Ethiopia a few
years ago?
What happened to President
Kennedy ?
What happened to Princess Grace
of Monaco
What happened to Cambridge
Crew in the 1984 Boat Race?
Who are the Boys in the Jamie
Bulgier affair ?
Who shot John Lennon ?

Public unknown

Public unknown

How did you spend last Xmas ?


What did you do yesterday ?
Name one person you met this
morning
Can you remember writing your
first letter?

OO
F

Context dependent
Personal known
Personal known
Personal known

Bruce, V. (1986). Influences of familiarity on the processing of faces.


Perception, 15(4), 387397.
Bruce, V., & Young, A. (1986). Understanding face recognition. British
Journal of Psychology, 77(Part 3), 305327.
Burton, A. M., Bruce, V., & Johnston, R. A. (1990). Understanding face
recognition with an interactive activation model. British Journal of
Psychology, 81(Pt 3), 361380.
Cermak, L. S., & OConnor, M. (1983). The anterograde and retrograde
retrieval ability of a patient with amnesia due to encephalitis. Neuropsychologia, 21(3), 213234.
Chan, D., Fox, N., & Rossor, M. (2002). Differing patterns of temporal
atrophy in Alzheimers disease and semantic dementia. Neurology,
58(5), 838.
Chan, D., Fox, N. C., Scahill, R. I., Crum, W. R., Whitwell, J. L.,
Leschziner, G., et al. (2001). Patterns of temporal lobe atrophy in semantic dementia and Alzheimers disease. Annals of Neurology, 49(4),
433442.
Cipolotti, L., Shallice, T., Chan, D., Fox, N., Scahill, R., Harrison, G.,
et al. (2001). Long-term retrograde amnesia. The crucial role of the
hippocampus. Neuropsychologia, 39(2), 151172.
Colchester, A., Kingsley, D., Lasserson, D., Kendall, B., Bello, F., Rush,
C., et al. (2001). Structural Mri volumetric analysis in patients with
organic amnesia. 1. Methods and comparative findings across diagnostic groups. Journal of Neurology, Neurosurgery and Psychiatry,
71(1), 1322.
Coughlan, A. K., & Warrington, E. K. (1981). The impairment of verbal
semantic memory: A single case study. Journal of Neurology, Neurosurgery and Psychiatry, 44(12), 10791083.
Dalla Barba, G., Cappelletti, J. Y., Signorini, M., & Denes, G. (1997).
Confabulation: Remembering another past, planning another future.
Neurocase, 3(6), 425435.
Ellis, A. W., & Morrison, C. M. (1998). Real age-of-acquisition effects in
lexical retrieval. Journal of Experimental Psychology, Learning Memory and Cognition, 24(2), 515523.
Ellis, A. W., & Ralph, M. A. L. (2000). Age of acquisition effects in
adult lexical processing reflect loss of plasticity in maturing systems:
Insights from Connectionist networks. Journal of Experimental Psychology, Learning Memory and Cognition, 26(5), 11031123.
Gabrieli, J. D., Cohen, N. J., & Corkin, S. (1988). The impaired learning of semantic knowledge following bilateral medial temporal-lobe
resection. Brain and Cognition, 7(2), 157177.
Gainotti, G., Barbier, A., & Marra, C. (2003). Slowly progressive defect in
recognition of familiar people in a patient with right anterior temporal
atrophy. Brain, 126, 792803.
Galton, C. J., Patterson, K., Graham, K., Lambon-Ralph, M. A., Williams,
G., Antoun, N., et al. (2001). Differing patterns of temporal atrophy in Alzheimers disease and semantic dementia. Neurology, 57(2),
216225.
Graham, K. S., Pratt, K. H., & Hodges, J. R. (1998). A reverse temporal
gradient for public events in a single case of semantic dementia.
Neurocase, 4(6), 461470.
Greene, J. D., & Hodges, J. R. (1996). The fractionation of remote memory. evidence from a longitudinal study of dementia of Alzheimer
type. Brain, 119(Pt 1), 129142.
Hirsh, K. W., & Ellis, A. W. (1994). Age of acquisition and lexical processing in aphasia: A case study. Cognitive Neuropsychology, 11(4),
435458.
Hodges, J. R., & McCarthy, R. A. (1995). Loss of remote memory: A
cognitive neuropsychological perspective. Current Opinion in Neurobiology, 5(2), 178183.
Hodgson, C., & Ellis, A. W. (1998). Last in first to go: Age of acquisition
and naming in the elderly. Brain and Language, 64(1), 146163.
Kali, S., & Dayan, P. (2004). Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nature Neuroscience, 7(3), 286294.

PR

Example items from the MACQ test

989

TE
D

987

Appendix A

EC

986

15

NSY 1861 117

990
991
992
993
994
995
996
997
998
999
1000
1001
1002
1003
1004
1005
1006
1007
1008
1009
1010
1011
1012
1013
1014
1015
1016
1017
1018
1019
1020
1021
1022
1023
1024
1025
1026
1027
1028
1029
1030
1031
1032
1033
1034
1035
1036
1037
1038
1039
1040
1041
1042
1043
1044
1045
1046
1047
1048
1049
1050
1051
1052
1053
1054

1061
1062
1063
1064
1065
1066
1067
1068
1069
1070
1071
1072
1073
1074
1075
1076
1077
1078
1079
1080
1081
1082
1083
1084
1085
1086
1087
1088
1089
1090
1091
1092
1093
1094
1095
1096
1097
1098
1099
1100
1101
1102
1103
1104
1105
1106
1107
1108
1109
1110
1111
1112
1113
1114
1115
1116
1117
1118
1119
1120
1121

Nader, K. (2003). Memory traces unbound. Trends in Neurosciences,


26(2), 6572.
Reed, J. M., & Squire, L. R. (1998). Retrograde amnesia for facts
and events: Findings from four new cases. Journal of Neuroscience,
18(10), 39433954.
Rempel-Clower, N. L., Zola, S. M., Squire, L. R., & Amaral, D. G.
(1996). Three cases of enduring memory impairment after bilateral
damage limited to the hippocampal formation. Journal of Neuroscience, 16(16), 52335255.
Rusconi, M. L., Zago, S., & Basso, A. (1997). Semantic amnesia without
dementia: Documentation of a case. Italian Journal of Neurological
Sciences, 18(3), 167171.
Sanders, H. I., & Warrington, E. K. (1971). Memory for remote events
in amnesic patients. Brain, 94(4), 661668.
Schacter, D. L., Verfaellie, M., & Anes, M. D. (1997). Illusory memories in amnesic patients: Conceptual and perceptual false recognition.
Neuropsychology, 11(3), 331342.
Schmolck, H., Kensinger, E. A., Corkin, S., & Squire, L. R. (2002).
Semantic knowledge in patient H.M. and other patients with bilateral medial and lateral temporal lobe lesions. Hippocampus, 12(4),
520533.
Spiers, H. J., Maguire, E. A., & Burgess, N. (2001). Hippocampal amnesia. Neurocase, 7(5), 357382.
Snowden, J. S., Griffiths, H. L., et al. (1995). Autobiographical experience
and word meaning. Memory, 3(3/4), 225246.
Snowden, J. S., & Neary, D. (2002). Relearning of verbal labels in semantic dementia. Neuropsychologia, 40(10), 17151728.
Squire, L. R. (1998). Memory Systems. C. Royal Academy Sciences III,
321(23), 153156.
Squire, L. R., & McKee, R. D. (1993). Declarative and nondeclarative
memory in opposition: When prior events influence amnesic patients
more than normal subjects. Memory and Cognition, 21(4), 424430.
Squire, L. R., & Zola, S. M. (1998). Episodic, memory, semantic, memory
and amnesia. Hippocampus, 8(3), 205211.
Stefanacci, L., Buffalo, E. A., Schmolck, H., & Squire, L. R. (2000).
Profound amnesia after damage to the medial temporal lobe: A neuroanatomical and neuropsychological profile of patient E.P. Journal
of Neuroscience, 20(18), 70247036.
Talbot, P. R., Snowden, J. S., Lloyd, J. J., Neary, D., & Testa, H. J.
(1995). The contribution of single photon emission tomography to
the clinical differentiation of degenerative cortical brain disorders.
Journal of Neurology, 242(9), 579586.
Tulving, E. (1987). Multiple memory systems and consciousness. Human
Neurobiology, 6(2), 6780.
Tulving, E. (2001). Episodic memory and common sense: How far apart?
Philosophical Transactions of the Royal Society of London Series BBiological Sciences, 356(141), 15051515.
Van der Linden, M., Cornil, V., Meulemans, T., Ivanoiu, A., Salmon, E.,
& Coyette, F. (2001). Acquisition of a novel vocabulary in an amnesic
patient. Neurocase, 7(4), 283293.
Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van
Paesschen, W., & Mishkin, M. (1997). Differential effects of early
hippocampal pathology on episodic and semantic memory. Science,
277(5324), 376380.
Verfaellie, M., Koseff, P., & Alexander, M. P. (2000). Acquisition of
novel semantic information in amnesia: Effects of lesion location.
Neuropsychologia, 38(4), 484492.
Verfaellie, M., Reiss, L., & Roth, H. L. (1995). Knowledge of new english vocabulary in amnesia: An examination of premorbidly acquired
semantic memory. Journal of the International Neuropsychological
Society, 1(5), 443453.
Viskontas, I. V., McAndrews, M. P., & Moscovitch, M. (2000). Remote episodic memory deficits in patients with unilateral temporal
lobe epilepsy and excisions. Journal of Neuroscience, 20(15), 5853
5857.
Warrington, E. K. (1975). The selective impairment of semantic memory.
Quarterly Journal of Experimental Psychology, 27(4), 635657.

PR

1060

TE
D

1059

EC

1058

RR

1057

Kapur, N. (1999). Syndromes of retrograde amnesia: A conceptual and


empirical synthesis. Psychological Bulletin, 125(6), 800825.
Kitchener, E. G., & Hodges, J. R. (1999). Impaired knowledge of famous
people and events with intact autobiographical memory in a case
of progressive right temporal lobe degeneration: Implications for the
organisation of remote memory. Cognitive Neuropsychology, 16(6),
589607.
Kitchener, E. G., Hodges, J. R., & McCarthy, R. (1998). Acquisition of
post-morbid vocabulary and semantic facts in the absence of episodic
memory. Brain, 121(Pt 7), 13131327.
Kopelman, M. D. (2002). Disorders of memory. Brain, 125(Part 10),
21522190.
Kopelman, M. D., Lasserson, D., Kingsley, D. R., Bello, F., Rush, C.,
Stanhope, N., et al. (2003). Retrograde amnesia and the volume of
critical brain structures. Hippocampus, 13(8), 879891.
Kopelman, M. D., Stanhope, N., & Kingsley, D. (1999). Retrograde amnesia in patients with diencephalic. Temporal lobe or frontal lesions.
Neuropsychologia, 37(8), 939958.
Kopelman, M. D., Wilson, B. A., & Baddeley, A. D. (1989). The autobiographical memory interview: A new assessment of autobiographical
and personal semantic memory in amnesic patients. Journal of Clinical and Experimental Neuropsychology, 11(5), 724744.
Laws, K. R., McKenna, P., & McCarthy, R. (1995). Delusions about
people. Neurocase, 1, 349362.
McCarthy, R. A., Evans, J. J., & Hodges, J. R. (1996). Topographic amnesia: Spatial memory disorder, perceptual dysfunction, or category
specific semantic memory impairment? Journal of Neurology, Neurosurgery and Psychiatry, 60(3), 318325.
McCarthy, R. A., & Warrington, E. K. (1992). Actors but not scripts:
The dissociation of people and events in retrograde amnesia. Neuropsychologia, 30(7), 633644.
McClelland, J. L., McNaughton, B. L., & OReilly, R. C. (1995). Why
there are complementary learning systems in the hippocampus and
neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review, 102(3),
419457.
McNeil, J. E., & Warrington, E. K. (1991). Prosopagnosia: A reclassification. Quarterly Journal of Experimental Psychology Section a-Human
Experimental Psychology, 43(2), 267287.
McNeil, J. E., & Warrington, E. K. (1993). Prosopagnosia: A face-specific
disorder. Quarterly Journal of Experimental Psychology Section aHuman Experimental Psychology, 46(1), 110.
Milner, B. (1972). Disorders of learning and memory after temporal lobe
lesions in man. Clinical Neurosurgery, 19, 421446.
Mishkin, M., Suzuki, W. A., Gadian, D. G., & Vargha-Khadem, F. (1997).
Hierarchical organization of cognitive memory. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences,
352(136), 14611467.
Mishkin, M., Vargha-Khadem, F., & Gadian, D. G. (1998). Amnesia
and the organization of the hippocampal system. Hippocampus, 8(3),
212216.
Moscovitch, M., & Nadel, L. (1998). Consolidation and the hippocampal
complex revisited: In defense of the multiple-trace model. Current
Opinion in Neurobiology, 8(2), 297300.
Moss, H. E., Kopelman, M. D., Cappelletti, M., De Mornay Davies, P.,
& Jaldow, E. (2003). Lost for words or loss of memories? Autobiographical memories in semantic dementia. Cognitive Neuropsychology, 20(8), 7073.
Mummery, C. J., Patterson, K., Wise, R. J., Vandenbergh, R., Price, C.
J., & Hodges, J. R. (1999). Disrupted temporal lobe connections in
semantic dementia. Brain, 122(Part 1), 6173.
Nadel, L., & Moscovitch, M. (1997). Memory Consolidation. Retrograde
Amnesia and the Hippocampal Complex. Current Opinion in Neurobiology, 7(2), 217227.
Nadel, L., Samsonovich, A., Ryan, L., & Moscovitch, M. (2000). Multiple
trace theory of human memory: Computational, neuroimaging, and
neuropsychological results. Hippocampus, 10(4), 352368.

CO

1056

UN

1055

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

OO
F

16

NSY 1861 117

1122
1123
1124
1125
1126
1127
1128
1129
1130
1131
1132
1133
1134
1135
1136
1137
1138
1139
1140
1141
1142
1143
1144
1145
1146
1147
1148
1149
1150
1151
1152
1153
1154
1155
1156
1157
1158
1159
1160
1161
1162
1163
1164
1165
1166
1167
1168
1169
1170
1171
1172
1173
1174
1175
1176
1177
1178
1179
1180
1181
1182
1183
1184
1185
1186
1187
1188

R. McCarthy et al. / Neuropsychologia xxx (2004) xxxxxx

1196
1197

OO
F

1195

PR

1194

TE
D

1193

EC

1192

Westmacott, R., & Moscovitch, M. (2001). Names and words without


meaning: Incidental postmorbid semantic learning in a person with
extensive bilateral medial temporal damage. Neuropsychology, 15(4),
586596.
Westmacott, R., & Moscovitch, M. (2002). Temporally graded semantic
memory loss in amnesia and semantic dementia: Further evidence for
opposite gradients. Cognitive Neuropsychology, 19(2), 135163.
Wilson, B., & Baddeley, A. (1988). Semantic, episodic, and autobiographical memory in a postmeningitic amnesic patient. Brain and Cognition,
8(1), 3146.

RR

1191

Warrington, E. K. (1979). Neuropsychological evidence for multiple memory systems. Ciba Foundation Symposium, 69, 153166.
Warrington, E. K., & Duchen, L. W. (1992). A re-appraisal of a
case of persistent global amnesia following right temporal lobectomy: A clinico-pathological study. Neuropsychologia, 30(5), 437
450.
Warrington, E. K., & McCarthy, R. A. (1988). The fractionation of retrograde amnesia. Brain and Cognition, 7(2), 184200.
Warrington, E. K., & Weiskrantz, L. (1968). A study of learning and
retention in amnesic patients. Neuropsychologia, 6, 283291.

CO

1190

UN

1189

17

NSY 1861 117

1198
1199
1200
1201
1202
1203
1204
1205
1206
1207

You might also like