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Neurocase: The Neural Basis of Cognition
Publication details, including instructions for authors and subscription information:
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Topographical, Autobiographical and Semantic Memory
in a Patient with Bilateral Mesial Temporal and
Retrosplenial Infarction
a

Ilana J. Hepner , Armin Mohamed

b c

, Michael J. Fulham

b c

& Laurie A. Miller

c d

a

Macquarie Centre for Cognitive Science , Macquarie University , Sydney, Australia

b

Department of PET and Nuclear Medicine , Royal Prince Alfred Hospital , Sydney, Australia

c

Faculty of Medicine , University of Sydney , Sydney, Australia

d

Neuropsychology Unit , Royal Prince Alfred Hospital , Sydney, Australia
Published online: 25 Aug 2010.

To cite this article: Ilana J. Hepner , Armin Mohamed , Michael J. Fulham & Laurie A. Miller (2007) Topographical,
Autobiographical and Semantic Memory in a Patient with Bilateral Mesial Temporal and Retrosplenial Infarction, Neurocase:
The Neural Basis of Cognition, 13:2, 97-114, DOI: 10.1080/13554790701346297
To link to this article: http://dx.doi.org/10.1080/13554790701346297

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Neurocase (2007) 13, 97–114
http://www.psypress.com/neurocase
ISSN: 1355-4794 print / 1465-3656 online
DOI: 10.1080/13554790701346297

Topographical, Autobiographical and Semantic Memory
in a Patient with Bilateral Mesial Temporal
and Retrosplenial Infarction
NNCS

ILANA J. HEPNER1, ARMIN MOHAMED2,3, MICHAEL J. FULHAM2,3 and LAURIE A. MILLER3,4
Retrograde Memory Subsequent to Bilateral MTL Lesions

Downloaded by [The University of Manchester Library] at 10:15 18 December 2014

1

Macquarie Centre for Cognitive Science, Macquarie University, Sydney, Australia
Department of PET and Nuclear Medicine, Royal Prince Alfred Hospital, Sydney, Australia
3
Faculty of Medicine, University of Sydney, Sydney, Australia
4
Neuropsychology Unit, Royal Prince Alfred Hospital, Sydney, Australia
2

According to Consolidation Theory (Squire, 1992, Psychological Review, 99, 195; Squire & Alvarez, 1995, Current Opinion in
Neurobiology, 5, 169), the mesial temporal lobes have a time-limited role in the maintenance, storage and retrieval of retrograde
declarative memories, such that they are not necessary for recalling remote memories. In contrast, proponents of the Multiple Trace
Theory (Fuji, Moscovitch, & Nadel, 2000, Handbook of neuropsychology, 2nd ed., p 223, Amsterdam, New York: Elsevier; Nadel &
Moscovitch, 1999, Current Opinion in Neurobiology, 7, 217) posit that the mesial temporal lobe (MTL) is necessary for remembering
detailed autobiographical and topographical material from all time periods. A third theory of hippocampal function, the Cognitive Map
Theory (O’Keefe & Nadel, 1978, The hippocampus as a cognitive map. Oxford: Clarendon), states that the hippocampus is involved in
the processing of allocentric spatial representations. The precise role of the MTL in remote memory has been difficult to elucidate, as the
majority of studies present cases with widespread brain damage that often occurred many years prior to testing. We investigated
retrograde autobiographical, semantic and topographical memories in a subject (SG) who had recently sustained infarctions confined to
the MTL and retrosplenial region bilaterally. Inconsistent with the predictions of Cognitive Map Theory, memory for spatial maps that
were learned in the past was preserved. Additional testing indicated that SG suffered from a landmark agnosia, which affected remotely
and recently acquired information equally. SG was also poor at imagining which direction he would have to turn his body to move from
one landmark to another. In accordance with Consolidation Theory, SG performed similarly to control subjects for remote time periods on
various measures of retrograde autobiographical memory and demonstrated intact knowledge regarding famous faces and vocabulary
terms that were acquired in the past. In contrast, memory for remote public events was impaired. The current findings indicate that the
mesial temporal and/or retrosplenial regions have little role to play in memory for remotely acquired spatial maps, autobiographical
memories, famous faces or vocabulary terms. However, the findings for landmark naming, directional calculations between landmarks
and knowledge of public events suggest that the MTL and/or retrosplenial cortices remain important for accessing these types of
memories indefinitely.
Keywords: Brain lesions, retrograde memory, cerebrovascular accident, Consolidation Theory, Multiple Trace Theory, Cognitive Map
Theory, stroke

Introduction
There are a number of competing theories about the way in
which autobiographical, topographical and semantic memories are represented in the brain. Most emphasise some role of

the hippocampus and adjacent structures, but the time course
and nature of this role has been debated. There are only three
cases in the published literature with bilateral hippocampal
damage that have had the relationships between these three
aspects of retrograde memory investigated, and they provide

This research was in part supported by a Research Award for Areas and Centres of Excellence, a Macquarie Centre for Cognitive Science
Award and a Macquarie University Postgraduate Research Fund, awarded to the first author. We wish to acknowledge Professors John
Hodges, Morris Moscovitch and Larry Squire as well as Drs Ken Cheng, Judith Homewood and Suncica Lah and Ms Kathy Gray for
helpful discussions regarding the subject matter and Dr Alan Taylor for his assistance with the statistical analyses. We would like to thank
Associate Professor John Watson for access to SG. We also greatly appreciate the participation of all the subjects in this study and would
like to thank them for their time and interest.
Address correspondence to Ilana J. Hepner, Westmead Cognition Clinic, Westmead Hospital, Sydney, Australia. Tel: +612 9845 5080.
Fax: +612 9687 1429. E-mail: Ilana_Hepner@wsahs.nsw.gov.au
© 2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business

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I.J. HEPNER ET AL.

somewhat conflicting results. In this paper, we review the
findings from these cases as well as their limitations and provide new findings from a fourth case.
Squire and his colleagues (Reed & Squire, 1998; Stefanacci,
Buffalo, Schmolck, & Squire, 2000; Teng & Squire, 1999)
reported on subject EP, a 76-year-old man, who incurred
bilateral anterior MTL damage subsequent to an episode of
herpes simplex encephalitis. EP demonstrated a temporal gradient in his memory for topographical information and autobiographical episodes, such that his memory for his
childhood years was preserved. In contrast, he could not
recall any information about his current neighbourhood or
any autobiographical episodes from the past 50 years of his
life. Knowledge pertaining to news events, famous faces,
famous names and vocabulary that had been acquired during
his late twenties and onwards was found to be markedly
impaired. Unfortunately, this sort of knowledge was not sampled from the whole of his life span and so we do not know
the state of EP’s knowledge for information that he would
have acquired prior to his late twenties and a temporal gradient similar to the one found for autobiographical memories
cannot be ruled out.
Squire and his colleagues concluded that the findings from
EP support the predictions of the Consolidation Theory
(Squire, Cohen, & Nadel, 1984; Squire, 1992; Squire &
Alvarez, 1995). This theory posits that the hippocampus and
adjacent structures (dentate gyrus, subiculum and parahippocampal gyrus) direct the recall of recently acquired topographical, episodic and semantic memories, the various
components of which are maintained in a distributed neocortical network and are partially stored (Alvarez & Squire,
1994) or linked (Meeter & Murre, 2005; Murre, 1996) by the
hippocampal system. Over time, the remote memory
becomes independent of the mesial temporal lobe (MTL)
region through a process termed consolidation, and is sustained entirely by the neocortex.
Rosenbaum et al. (2000) found a different pattern of results
in a second patient, KC, a 49-year-old male, who had become
amnesic 18 years prior to testing as the result of a motorcycle
accident. KC had sustained widespread brain lesions that virtually encompassed both MTL and also involved left mesial
occipital-temporal, left frontal-parietal, right mesial frontal
and right parieto-occipital regions. KC was completely unable
to recall detailed autobiographical events for the whole of his
life, including his early years (Rosenbaum, McKinnon,
Levine, & Moscovitch, 2004a; Tulving, Schacter, McLachlan,
& Moscovitch, 1988; Tulving, Hayman, & Macdonald, 1991;
Westmacott, Leach, Freedman, & Moscovitch, 2001). In
terms of his topographical memory, Rosenbaum et al. (2000)
found that KC was impaired at distinguishing incidental landmarks in his own locality from those in nearby neighbourhoods (Tulving et al., 1988; Westmacott et al., 2001;
Rosenbaum et al., 2004a), but otherwise demonstrated intact
topographical knowledge. KC’s retrograde memory for
vocabulary terms and famous personality’s names was intact
except for those he should have learnt during the 5 years prior

to his injury (Westmacott & Moscovitch, 2002). His memory
for public events was not tested.
The findings for KC were interpreted as being in accordance with the predictions of Multiple Trace Theory (MTT,
Nadel & Moscovitch, 1997; Moscovitch & Nadel, 1998; Fujii,
Moscovitch, & Nadel, 2000). A central tenet of MTT is that
the hippocampal complex remains involved in the storage,
maintenance and retrieval of autobiographical episodes for as
long as the memories are in existence. Complete damage to
the MTL bilaterally is predicted to result in an equivalent
impairment of remote and recent memory for autobiographical incidents. MTT postulates that the hippocampus has no
long-term role in the maintenance of factual or semantic
knowledge and therefore only very recently acquired information should be compromised following a lesion involving this
structure. It should be noted, however, that inferences pertaining to brain-behaviour relationships drawn by the Rosenbaum
et al. (2000) study are limited by the fact that KC incurred
damage to several brain regions. This raises the possibility
that the observed deficits in incidental landmark recognition
and/or remote autobiographical event memory might be the
result of damage to regions outside the MTL.
The third case in the literature where all three domains of
retrograde memory were compared was TT, a 65-year-old
retired London taxi driver who suffered an episode of limbic
encephalitis associated with a series of complex partial and
tonic-clonic seizures during the course of his recovery
(Maguire, Nannery, & Spiers, 2006). Magnetic resonance
imaging (MRI) revealed damage throughout the length of
both hippocampi. The entorhinal, perirhinal and parahippocampal cortices appeared relatively preserved in the context of
some generalised atrophy. TT’s retrograde topographical
memory was assessed through use of a virtual reality replication of London and his performance was compared to other
taxi drivers of a similar age. Interestingly, TT was able to
recall routes that primarily consisted of main artery roads (“A
roads”), but performed poorly when he was required to navigate in areas that contained few or no “A roads”. Knowledge
of landmarks and directions was intact. Maguire et al. (2006)
concluded that the hippocampus plays a vital role in the recollection of remotely learned spatial details, consistent with
the predictions of MTT. Similar to KC, and in contrast to EP,
TT demonstrated a complete loss of memory for autobiographical incidents across his lifespan. Consistent with findings from EP, knowledge of public events was impaired,
although the authors do not provide information with regard
to TT’s pattern of performance across each decade. In contrast to the findings for EP, however, TT’s knowledge of
famous faces was found to be intact.
Amongst these three patients there are varying degrees of
impairment in topographical, autobiographical and semantic
retrograde memory and the reason for this is not clear. It is
possible that etiology and/or site of lesion contribute to the
different profiles of impairment. As such, the exploration of
patterns of impairment in patients with different types of
MTL damage should help to resolve this issue.

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RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS
The neural organisation of topographical memory has been
described by two main theories. One, the Cognitive Map
Theory (O’Keefe & Nadel, 1978), proposes that the hippocampus is involved in the mapping of space, where the locations of objects are defined relative to the environment
(allocentric spatial representation). According to this theory,
observer dependent (egocentric) spatial representations are
thought to be processed by the posterior parietal cortices. An
alternative conceptualisation of the neural representation of
large scale space has been proposed by Aguirre and
D’Esposito (1999). Based on a review of the literature, they
argued that the inferior temporo-occipital regions are important for the recognition of previously familiar landmarks.
Way-finding, they argued, can be achieved using a variety of
strategies involving allocentric and egocentric processes in
conjunction with landmark recognition. As such, a preservation of way-finding in familiar environments might be
expected even when the hippocampus is dysfunctional. They
also concluded that the retrosplenial region calculates the
observer’s orientation with respect to the external environment and damage to this region is predicted to result in
“heading disorientation”. The preserved memory for routes
and layouts of remotely learned environments observed for
EP and KC, was interpreted by Teng and Squire (1999) and
Rosenbaum et al. (2000) as inconsistent with Cognitive Map
Theory, but the findings may well fit into Aguirre and
D’Esposito’s model. Unfortunately, in EP and KC, not all
aspects of their model were explored. TT’s intact knowledge
of landmarks, main routes and directional information was
also judged to be inconsistent with the Cognitive Map Theory. However, his data were not entirely consistent with
Aguirre & D’Esposito’s model either, as seen in his poor navigational ability on local roads in the face of seemingly focal
bilateral hippocampal damage.
In order to evaluate these theories of memory representation, we investigated topographical, autobiographical and
semantic memory in a patient (SG) who had recently developed bilateral lesions affecting the mesial temporal and the
retrosplenial regions subsequent to sequential infarctions.
Impairments in all allocentric aspects of topographical memory would be evidence for the Cognitive Map Theory
(O’Keefe & Nadel, 1978). In contrast, based on Aguirre and
D’Esposito’s model, SG’s lesion should cause deficits in
heading orientation, but possibly spare knowledge of routes.
Aguirre and D’Esposito’s (1999) model would also predict
deficits in landmark recognition, although according to
Rosenbaum et al. (2000) this should only affect recognition
of incidental landmarks. Furthermore, evidence of a temporal
gradient in autobiographical memory would indicate support
for the Consolidation Theory of long-term memory, whereas
compromised recall of memories across all time periods
would substantiate the claims of MTT. Due to the restricted
nature of SG’s temporal lobe lesions, both MTT and Consolidation Theory would predict minimal disruption to his retrograde semantic stores, with recently acquired memories more
vulnerable than those learnt in the remote past.

99

Case description
When he first presented in May 1998, SG was a 62-year-old
right handed male, with a Bachelor of Science and Engineering degree, who had retired 6 years earlier from his job as
Telecommunications Engineer/General Manager of a multinational company. He had suffered an infarct in the territory of
the right posterior cerebral artery, associated with left visual
field difficulties, which resolved completely soon after. Prior
to and after this infarction SG was on antihypertensive medication. There were no known premorbid neurological or psychiatric conditions. In July 2001, SG suffered a second infarct,
in the territory of the left posterior cerebral artery. Neurological examination revealed a right upper quadrantanopia, which
again proved transient. Limb functions were normal.
In October 2001, SG and his wife were interviewed at
Royal Prince Alfred Hospital. The main complaint was of
poor anterograde memory since the second stroke. In addition, SG’s wife reported that her husband would become lost
in previously familiar environments such as the streets
around their home and the local shopping centre. By contrast,
she described his premorbid navigational abilities as “excellent”. Conversational abilities were unaltered and he retained
his knowledge of Spanish and French. At reassessment in
October 2002, SG’s wife thought that her husband’s functioning had remained relatively stable. All testing reported in
the current study was conducted after the second stroke (in
2002 and 2003).
Magnetic resonance imaging (MRI) in July 2001 revealed
a previously sustained infarction of the right mesial temporal
cortex as well as an acute cerebral infarction involving the
mesial aspect of the left temporal lobe and the occipital lobes
bilaterally (Figure 1). Neuroradiological review of the MRI
data indicated an old cortical infarct involving all of the hippocampus and much of the parahippocampal gyrus, entorhinal cortex and perirhinal cortex on the right. Additional
signal change, consistent with more recent damage was
noted in the right retrosplenial region. Within the left
hemisphere, all of these same regions were affected, with
more extensive changes suggested in the posterior parahippocampal/retrosplenial region. In contrast, the temporal
poles and inferior cortex lateral to the parahippocampal gyri
is largely spared.
For the purposes of the study, fluoro-deoxyglucose
positron emission tomography (FDG-PET) was conducted
in January 2003 (Figure 2). Visual inspection of the FDGPET data by a neurologist (AM) revealed glucose hypometabolism in a number of regions. The largest of these
involved the entire right mesial temporal lobe with some
suggestion of dilatation of the right temporal horn and
body of the lateral ventricle, particularly posteriorly.
Additional areas of reduced glucose metabolism included
the left entorhinal region and hippocampus as well as the
retrosplenial region bilaterally. Glucose metabolism was
relatively spared in the prefrontal cortex and in both
thalami.

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I.J. HEPNER ET AL.

Fig. 1. MR FLAIR images taken soon after the second stroke
showing left/right reversed coronal slices moving more anteriorly
from the top left to the bottom right of the figure. There is increased
signal and atrophy due to infarction in the right hippocampus (A); as
well as signal change in the head and body of the left hippocampus
(B); retrosplenial regions bilaterally (C); left parahippocampal gyrus
and mesial occipital cortex (D); and right inferior occipital cortex (E).

For quantitative analysis, the FDG-PET data were transformed to Talairach and Tournoux (1988) space and measurements of cerebral glucose metabolism (CMRGlu) in four brain
regions (left and right retrosplenial regions, left and right parahippocampal gyri) were taken. The CMRGlu measurements
were then compared with data procured in a similar fashion from
25 male normal control (NC) subjects, aged 65–75. In order to
control for inter-individual variations in total brain volume, the
CMRGlu for each of the four brain regions was divided by the
CMRGlu obtained for the pons for each individual brain. Subsequent to this, modified t-tests were performed according to a
formula proposed by Crawford and his colleagues (Crawford
& Howell, 1998; Crawford & Garthwaite, 2002) for each of
the four brain regions. Significant differences in glucose
metabolism were found between SG’s brain and NCs for the
right (p < .01) and left (p < .0167) retrosplenial cortices and
right parahippocampal region (p < .012). The left parahippocampal region did not differ significantly from those of controls.

Standard neuropsychological assessment of SG
Three and 15 months after his second stroke, SG underwent
neuropsychological assessment (Table 1). His estimated premorbid Full Scale IQ was 122, in the superior range (National
Adult Reading Test – NART, Nelson, 1982). Scores on tests
of general knowledge, word definitions, mental arithmetic,

Fig. 2. FDG PET scan showing (from top to bottom of the figure,
inferior to more superior- and left/right reversed) slices parallel to the
main axis of the hippocampus. These reveal glucose hypometabolism
in: the posterior parahippocampal gyri (A); left entorhinal cortex (B);
right entorhinal cortex (C); right occipital pole (D); the right
hippocampus from the head (E) to the tail (F); the body of the left
hippocampus (G); and retrosplenial regions (H) (L>R). This figure is
available to subscribers in color: Please visit the Journal’s website at
http://www.psypress.com/neurocase.

verbal abstract reasoning, visuoconstruction and immediate
attention span were consistent with this expectation. Visuoperceptual and visuospatial skills along with mental flexibility and conceptual problem solving were found to be intact.
SG was also proficient in producing rote learned sequences,
as assessed by the Mental Control subtest of the Wechsler
Memory Scale – Revised (WMS-R, Wechsler, 1987).
As can be seen in Table 1, SG’s anterograde memory for
both visual and verbal material was severely impaired. He
sometimes denied having heard or seen material that had
been presented 30 min earlier.

Normal Control subjects
On the experimental measures, SG’s performance was compared with that of 11 NC subjects (six males and five
females) who were chosen as approximate matches for age,
intellectual ability and level of education. Table 2 presents
the demographics for these subjects.
This study was approved by the ethics committees of the
Central Sydney Area Health Service and Macquarie University. All subjects gave their informed consent to participate.

RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS

101

Table 1. Summary of SG’s performance on clinical measures of cognitive ability
3 months post second stroke

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Measure

Raw Score

WAIS-R Information
WAIS-R Vocabulary
WAIS-R Arithmetic
WAIS-R Similarities
WAIS-R Block Design
WAIS-R Digit Span Forwards
WAIS-R Digit Span Backwards
WMS-R Visual Memory Span Forwards
WMS-R Visual Memory Span Backwards
VOSP Incomplete Letters
VOSP Cube Analysis
WCST Categories
WCST Failure To Maintain Set
WCST Perseverative Errors
WCST Total Trials
WMS-R Mental Control
WMS-R Information & Orientation
WMS-R Logical Memory I
WMS-R Logical Memory II
WMS-R Visual Reproduction I
WMS-R Visual Reproduction II
RAVLT Learning Over Time
RAVLT Immediate Recall List A
RAVLT 20 min Delayed Recall List A
Rey Complex Figure Copy
Rey Complex Figure 30 min delay
Boston Naming Test
Semantic Battery Category Fluency
Semantic Battery Picture Naming
Semantic Battery Word Definitions
Semantic Battery Word Picture Matching

28
69
15
25
40
10
10
–
–
–
–
–
–
–
–
6/6
11/14
19
0
16
0
7
3
0
34
0
–
–
–
–
–

15 months post second stroke

Percentile

Raw Score

Percentile

99
>99
72–81
99
90–94
92
96
–
–
–
–
–
–
–
–
72–81
–
11–18
<1
<1
<1
6–10
1
<1
>16
<1
–
–
–
–
–

–
–
–
–
–
12
10
9
7
20
10
6
0
3
70
6/6
9/14
19
2
28
9
–
–
–
36
5
59
62
48/48
12/12
48/48

–
–
–
–
–
99
96
92
80
Pass
Pass
>16
>16
98
–
72–81
–
11–18
1
11–18
3–5
–
–
–
>16
1
98
31

WAIS-R, Wechsler Adult Intelligence Scale – Revised [Wechsler, 1981; Minnesota Older Adult Normative Study (MOANS) normative data (Ivnik, Malec, Smith,
Tangalos, & et al., 1992b)]; VOSP, Visual Object Space Perception Battery (Warrington & James, 1991); WCST, Wisconsin Card Sorting Test (Heaton, Chelune,
Talley, Kay, & Curtis, 1993); WMS-R, Wechsler Memory Scale – Revised, [Wechsler, 1987; MOANS normative data (Ivnik, Malec, Smith, Tangalos, & et al.,
1992c)]; RAVLT, Rey Auditory Verbal Learning Test [Rey, 1958; MOANS normative data (Ivnik, Malec, Smith, Tangalos, & et al., 1992a)]; Rey Complex
Figure, (Rey, 1941; Meyers & Meyers, 1995); Boston Naming Test (Kaplan, Goodglass & Weintraub, 1983); Semantic Battery (Hodges & Patterson, 1995)

Table 2. Demographics for SG and the NC subjects
Control Group

Age
Years of
Education
Estimated FSIQ1

SG

mean

sd

65
16

63.7
16.5

5.0
2.1

122

120.1

4.5

1

National Adult Reading Test (NART; Nelson, 1982); sd = standard deviation.

Statistical analyses
For each of the experimental measures, modified t-test analyses (Crawford & Howell, 1988) were conducted using a

programme developed by Crawford and Garthwaite (2002)
called “singlims”. Multiple comparisons were controlled for
using a sequentially rejective Bonferroni procedure proposed
by Holm (1979). Tasks were grouped according to cognitive
domain and this technique was applied multiple times.

Topographical memory
It has recently been proposed that various aspects of topographical memory can be differentially affected by damage to specific
brain areas (Aguirre & D’Esposito, 1999). Topographical skills
such as an individual’s ability to recognise landmarks (Hecaen,
Tzortzis, & Rondot, 1980; Whiteley & Warrington, 1978),
obtain directional information from them (Hirayama, Taguchi,
Sato, & Tsukamoto, 2003; Suzuki, Yamadori, Hayakawa, &

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I.J. HEPNER ET AL.

Fujii, 1998; Takahashi, Kawamura, Shiota, Kasahata, &
Hirayama, 1997) and recall routes (Bottini, Cappa, Geminiani,
& Sterzi, 1990; della Rocchetta, Cipolotti, & Warrington, 1996;
Paterson & Zangwill, 1945) have been considered in various
studies. However, few of these investigations have obtained
detailed neuroimaging data of their subjects, limiting the conclusions that can be drawn with regard to the neural underpinnings
of retrograde topographical memory. In light of this, we tested
SG on a battery of retrograde topographical memory tasks measuring landmark naming, heading orientation, landmark map
localisation and route recall to investigate the effect of mesial
temporal and retrosplenial lesions on these various abilities.
Performance on the tests of topographical memory was
thought possibly to be contingent upon a number of more
basic abilities including visual perception, visual imagery and
visuospatial skills. In order to establish whether any difficulties SG had on tests of topographical memory might be due to
an underlying deficiency in any of these domains, a number
of control tests were administered.
Subjects
All 11 NC subjects, as described in Table 2 had either grown up
in the Sydney metropolitan region or had moved to Sydney
three or more decades earlier. Their performance was compared
to SG, who had lived and worked in Sydney all of his life.
Tasks
Sydney City Test of topographical memory
All subjects were administered the Sydney City Test of
Topographical Memory (the “Sydney City Test”). Briefly,
this test is comprised of 50 photographs (21×15 cm) of landmarks (buildings, bridges and scenes) in Sydney. First, subjects were required to recall the name of each landmark.
Second, for incorrect items, the correct landmark name along
with the names of three other Sydney landmarks were presented to the subject, who was then asked to choose the
appropriate name from amongst the distracters.
A subset of these items (n = 15) was used to test heading
orientation. Subjects were asked to look at the photograph,
given the name of the landmark where necessary and asked to
imagine that they were standing in the same position as the
photographer. They were then asked (1) the direction of the
Queen Victoria Building (a very well known Sydney landmark) (i.e., “directly in front of me, behind me, to my right,
to my left, to the front and right, to the front and left, behind
and right or behind and left”) and (2) the cardinal direction
they were facing (i.e., north, south, east or west).
Eight pairs of relatively well-known landmarks were chosen
to serve as start and end points of the route recall subtest. The
landmarks that were chosen represented a good cross section of
the city of Sydney, and most routes were comprised of a combination of main and local roads. Responses were scored
according to the provision of correct street names or landmarks

(e.g., keep walking until you reach the supermarket), and correct number of turns. If the response from a subject was too
brief (eg. “walk down the main street and you’ll get there eventually”), the experimenter guided the subject through each
stage of the route by providing specific prompts (“so you’re at
landmark X/on street Y, what would be the first step you’d
take … then what would you do next?” and so on). The score
for each item was converted to the percentage correct and the
final route recall score was the average of these.
On the map localisation subtest, subjects were asked to
label a map of the city of Sydney, which had been edited
using Adobe® Photoshop® 7 to remove identifying information. Subjects were asked to label the map with the locations
of 16 landmarks (in response to being shown the picture and
given the name). The error score was a measure of distance
on the map (in cm) between the placement by the subject and
the true location. The total score was the sum of these error
measurements.
Control tasks
Building/scene matching. To evaluate a subject’s ability to
process architectural and scenic details, a building/scene
matching test was created. In each of 15 items, a target photograph (21×15 cm) of a non-famous building or scene was
presented to the subject along with 4 other photos (Figure 3).
One of those four photographs was the same building or
scene as the one depicted in the target photograph, but taken
from a slightly different angle. The other three photographs
were of closely matched distracters. Each subject was asked
to indicate which of the four photographs was the same as the
target photo.
Mental imagery. Two tests of mental imagery were administered, which required the subject to visualise either 26 common objects (Taller/Wider test: Kosslyn, Reiser, Farah, &
Fliegel, 1983) or 20 animals (Animal Tails Test: Martha
Farah, personal communication) and make judgements about
their physical properties. In the Taller/Wider Test, the subject
was asked to decide whether objects (e.g., a bow-tie or garbage bin) were taller than they were wide or wider than they
were tall. In the Animal Tails Test, subjects were asked to
think of different animals (e.g., a lion, deer etc) and determine whether they had a long or a short tail.
Mental rotation. The Space Thinking [Flags] Test (Thurstone
& Jeffrey, 1984) was used to assess mental rotation. In this
test, subjects are shown a target drawing of a flag along with
six other drawings of the same flag that were rotated at different angles, with some inverted on their axis. Subjects then
had to compare each of the six drawings with the target drawing and indicate whether they represented the same side as
the target flag or whether they were a mirror image. There
were 21 target items in total and each subject was given 5
min to complete as many items as possible.

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RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS

Fig. 3. An item from the Building/Scene Matching test. This figure is available to subscribers in color: Please visit the Journal’s website at
http://www.psypress.com/neurocase.

Results
Table 3 provides a summary of SG’s scores compared to
mean of the NC group on each of the six Sydney City subtests, using the sequential rejective Bonferroni procedure. His
ability to recall or recognise the names of landmarks was
found to be impaired relative to NCs (p < .008, p < .01,

respectively). SG also encountered difficulty on the test of
heading orientation when asked to give the direction of a
specific Sydney landmark when he imagined that he was
standing in front of another (p < .013). In contrast, SG’s
performance did not differ from the NCs when he was
asked which cardinal direction he would be facing as the

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I.J. HEPNER ET AL.

Table 3. Results for the Sydney City Test of Topographical
Memory and visual control tasks

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Task
Sydney City Test
Landmark Name
Recall (/50)
Landmark Name
Recognition (/50)
Direction of Second
Landmark (/15)
Cardinal
Direction (/15)
Landmark Map
Localisation
(Sum of Error
Measurements)
Spoken Route Recall
(percentage correct)
Visual Control Tasks
Building/Scene
Matching (/15)
Taller/Wider (/20)
Animal Tails (/26)
Mental Rotation

was unable to name were disclosed to him, he stated that he
was indeed familiar with these places and correctly determined the position of the second landmark for two of these
items.

SG’s Score

NC mean
(sd)

t

p

23*

41.0 (4.3)

−4.04

0.001

Remote versus recent topographical memory

36*

48.3 (1.7)

−6.76

0.000

7*

11.8 (1.0)

−4.70

0.000

9

11.4 (2.7)

−0.83

0.213

22.8

12.1 (9.6)

1.07

0.155

64.1

77.2 (8.5)

−1.48

0.084

13

12.9 (1.2)

0.1

0.472

19
22
44

19.2 (1.0)
23.6 (1.2)
37.2 (12.7)

−0.18
−1.30
0.52

0.431
0.112
0.309

Teng and Squire (1999) and Rosenbaum et al. (2000) hold
disparate views regarding the role of the hippocampus and
related mesial temporal structures in the processing of topographical memories, advocating the Consolidation Theory
(Squire, 1992; Squire & Alvarez, 1995) and MTT (Fujii
et al., 2000; Nadel & Moscovitch, 1997), respectively.
Following damage to these regions, Teng and Squire (1999)
argue that there will be a temporal gradient, with sparing
of the most remote topographical memories. In contrast,
Rosenbaum et al. (2000) maintain that the hippocampus plays
a role in memory for incidental landmarks acquired at any
point in one’s lifetime. Accordingly, we set out to look for a
temporal gradient in topographical memories and also to
determine whether SG would be able to recognise incidental
landmarks from his remote and recent past.

sd = standard deviation;
* = significantly different from the control group, based on calculations
performed using Crawford & Garthwaite’s (2001) programme ‘singlims’
and sequentially rejective Bonferroni corrections (Holm, 1979) (applied
separately for Sydney City subtests and set of visual control tasks).

photographer for the same items. Similarly, SG was able to
place landmarks on a map of Sydney as well as recall routes
between various landmarks within the Sydney metropolitan
region at a level comparable to NCs. On all control measures,
SG’s performance fell within normal limits (Table 3).
Comment
In summary, SG had difficulty remembering the names of
famous landmarks and their location with respect to other
landmarks when he had to imagine himself facing a particular direction. His impaired ability to recall or recognise the
names of well known landmarks from his home city was
unlikely to be due to underlying visual processing impairments, a general object agnosia or a naming problem, as he
performed normally on standardised neuropsychological
tests and experimental control tasks of these underlying
abilities. Similarly, his inability to make spatial judgements
regarding the position of one landmark in relation to his
position in front of another landmark was unlikely to be due
to a lack of knowledge about the 15 landmarks used in this
subtest, since he was able to place 13 of these relatively
accurately on the map and recall or recognise the names of
12 of them. Once the identities of the three items that he

Subjects
For the test of remote incidental topographical memory, SG’s
knowledge of the University of Sydney campus was compared with that of five male and two female NC subjects,
matched for age, education and estimated FSIQ (Table 4). SG
had attended the University of Sydney from the mid 1950s to
the early 1960s (aged 18–26) and had returned only to attend
his sons’ graduation ceremonies in 1992 and 1994. During
these visits he stated that he had not reacquainted himself
with the campus, but remained in the graduation hall. All
seven control subjects had attended the University of Sydney
during the same time period as SG, and had only returned
sporadically for conferences or reunions (none within the past
5 years). Like SG, they all stated that they had not reacquainted themselves with the University grounds during these
visits.
For the test of recent incidental topographical memory,
SG’s performance was compared with that of his wife and

Table 4. Demographics for the University of Sydney Test
Control Group

Age
Years of
Education
Estimated FSIQ1
1

SG

mean

sd

65
16

61.9
17.3

1.6
1.6

122

119.7

5.2

National Adult Reading Test (NART; Nelson, 1982); sd = standard deviation.

RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS
adult son. Both SG and his wife had lived in their current
neighbourhood for the past 40 years. Their son, aged 33 at the
time of testing, reported that although he had left the family
home 9 years earlier he had maintained regular contact with
his former neighbourhood.

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Tasks
To examine remote topographical memory, the Sydney
University Test was constructed. It consisted of 15 sets of four
colour photographs of landmarks (21×15 cm) (Figure 4). One of
the four photos in each set depicted a landmark from the University of Sydney that was present in the late 1950s. The other three
photographs were of closely matched distracters from outside of
Sydney. A number of these were obtained from the internet.
To assess more recent topographical memory, 20 sets of
four photographs (21×15 cm) were used in the Neighbourhood Test (Figure 5). Only one of the four photographs in
each set depicted an incidental landmark (house, intersection
or shop front) from SG’s current neighbourhood. Again, the
other three photographs were of closely matched distracters.
All photographs were taken by I.H. using a digital camera
and identifying information was removed. For each item on

105

the Sydney University and Neighbourhood Tests, subjects
were asked to indicate which of the four landmarks was part
of the University of Sydney or part of their home neighbourhood, respectively.

Results
SG’s ability to recognise both recent and remote landmarks as
familiar was impaired. Compared to NCs on the Sydney University Test, who averaged 13.7 correct, SG made only nine correct
choices (t = –4.63, p < .05). On the Neighbourhood Test, SG’s
wife and son both chose 18/20 items correctly. SG performed
much more poorly, making only 13/20 correct choices.

Comment
SG demonstrated a deficiency in recognising photographs of
incidental landmarks from both the remote and recent time
periods. These findings, combined with the results from the
previous section that demonstrated difficulties with naming
prominent landmarks yet intact perception of buildings and
scenes provide further evidence that SG’s symptomatology is

Fig. 4. An item from the Sydney University test. This figure is available to subscribers in color: Please visit the Journal’s website at http://
www.psypress.com/neurocase.

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106

I.J. HEPNER ET AL.

Fig. 5. An item from the Neighbourhood test. This figure is available to subscribers in color: Please visit the Journal’s website at http://
www.psypress.com/neurocase.

consistent with the features of a landmark agnosia, as predicted
by Aguirre and D’Esposito (1999). The results are somewhat
consistent with the proposal of Rosenbaum et al. (2000), that
deficient memory for topographical details, such as incidental
landmarks is a likely consequence of MTL damage.

complex is important in the recollection of detailed autobiographical incidents (rather than the gist of an autobiographical
experience) for the whole of a person’s lifetime, two measures of
autobiographical memory were administered to SG. The first
yielded data pertaining to personal semantic details and autobiographical incidents in moderate detail and the second required
the recall of highly detailed autobiographical incidents.

Autobiographical memory
We examined SG’s recall of personal semantic details and autobiographical incidents, with the intent to test the predictions of
two theories of long-term memory (Consolidation theory and
MTT). Proponents of Consolidation Theory (Squire, 1992;
Squire & Alvarez, 1995) would argue that SG should show a
time-limited loss of memory for personal semantic details and
autobiographical events, with remotely acquired memories
being intact. On the other hand, MTT (Fujii et al., 2000; Nadel &
Moscovitch, 1997) would predict poor recollection of remotely
and recently acquired autobiographical events in the context of a
restricted loss of memory for personal semantic details.
Because Moscovitch and colleagues (Levine, Svoboda, Hay,
Winocur, & Moscovitch, 2002; Moscovitch, Yaschyshyn,
Ziegler, & Nadel, 2000) have argued that the hippocampal

Subjects
All 11 NC subjects described in Table 1 performed the modified Crovitz Cue Technique (mCCT). Both tests of autobiographical memory were administered to SG in mid 2002.
Tasks
Autobiographical Memory Interview
The Autobiographical Memory Interview (AMI; Kopelman,
Wilson, & Baddeley, 1989) was used to assess SG’s memory
for personal semantic details and autobiographical incidents.
The personal-semantic scale of the AMI requires the subject
to provide personal semantic details, such as the name of the

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primary school they attended. Questions from the autobiographical-incident scale require the subject to recall specific
and detailed autobiographical incidents. These two domains
are assessed across three different life periods: Childhood,
Early Adult Life (until the age of 35 for SG) and Recent Life.
Normative data obtained from the manual were used to gauge
SG’s performance on this test.
mCCT
In a modified version of the Crovitz Cue Technique (Crovitz
& Schiffman, 1974; Cimino, Verfaellie, Bowers, & Heilman,
1991) subjects were presented with each of four cue words
(happy, afraid, angry and surprised) and were asked to recall a
specific and detailed autobiographical incident that the word
brought to mind. They were first instructed that the incident
was to have occurred between the ages of 0 and 12 years of
age (“Childhood”). This procedure was then repeated, using
three other time periods: 13–21 years of age (“Teenage/Young
Adult”); 1993–1997 (the 5 years preceding SG’s first stroke);
and the most recent 5 years (post first stroke). If the subject
provided only scant detail, prompts such as “Can you tell me
more about that?”, or “Who was there?” etc., were used.
Responses were taped and then transcribed. Scoring was conducted by an independent rater who was blind to subject
group. Responses were scored out of a possible seven points
with respect to whether they included details about who was
involved (1 point), where the event took place (1 point), when
the event took place (1 point) and what had occurred (2 points).
One point was also awarded if the memory described a specific
episode and another if it was clearly within the specified time
period. Responses were also scored according to the number
of prompts required. The questions ranged from general probing (“can you think of a specific incident?”) to more specific
prompts (e.g., “who else was there?”, “where were you at the
time?” and “what happened next”).

Fig. 6. SG’s performance on the Modified Crovitz Technique across
four time periods, compared with NCs. *p < .007. Error bars
indicate the standard error of the mean.

Recall of autobiographical events from the 5 years prior to
his first stroke (1993–1997) although lower than the NC
mean, was not significantly impaired (t = –1.61, ns). It may
be important to note, however, that compared with NCs, SG
required significantly more prompting to generate complete
memories of incidents for the 5 years prior to his first stroke
only (t = 3.55, p < .006) (Figure 7).
Comment

Results

As assessed by the AMI, SG was able to recall personal
semantic details from his own past across all time periods.
Neither MTT nor Consolidation Theory would have predicted complete preservation of personal semantic memory.
Two possibilities may explain SG’s intact performance on
this measure. First, it may be that a remnant of preserved
entorhinal or other anterior mesial temporal tissue was
capable of sustaining the retrieval of personal semantic
details. In support of this, Kapur and Brooks (1999)
reported preserved memory for personal semantic details in
two patients with restricted bilateral hippocampal damage

SG’s autobiographical memories were all verified by his wife.
SG’s performance on the personal semantic scale on the AMI
fell within normal limits, as stated in the manual, for all three
time periods. (Childhood = 16.5/21; Early Adult Life = 21/21;
Recent Life = 19/21). His scores on the autobiographical incident scale for childhood and early adult time periods were also
well within the normal range (Childhood = 7/9; Early Adult
Life = 8/9). His score (6/9) on the recall of autobiographical
incidents from the recent time period was rated in the borderline
range (between 1 and 2 standard deviations from the control
mean). This period covered the year since his second stroke.
Similarly, on the mCCT, SG was able to recall detailed
autobiographical incidents from the two remote time periods
(Childhood: t = 0.39, ns; Teenage/Young Adult: t = 0.49, ns)
(see Figure 6). SG’s recall of events that occurred within the
most recent 5 years in response to cue words, however, was
significantly impaired relative to NCs (t = –4.70, p < .006).

Fig. 7. Number of prompts required by SG and NCs, for each time
period on the Modified Crovitz Cue Technique. *p < .006. Error
bars indicate the standard error of the mean.

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I.J. HEPNER ET AL.

that was incurred subsequent to an episode of limbic
encephalitis. Second, a more sensitive test of personalsemantic memory might have detected some subtle deficits,
since other authors have commented on the reduced sensitivity of the AMI for both personal semantic details and
events (Eslinger, 1998; Kapur & Brooks, 1999; Manes,
Hodges, Graham, & Zeman, 2001).
SG’s recall of autobiographical events for remote time
periods (childhood and teenage/young adult years) was
within normal limits, as measured by the AMI and mCCT.
Furthermore, his recollections were as detailed as those provided by NCs and he did not require significantly more
prompts to elicit these memories. It is unlikely that these
memories were semanticised or over-rehearsed, as SG’s wife
confirmed that the episodes that SG had recalled were not a
recurring topic of discussion within their family.
Although the quality of SG’s responses on the mCCT for
the years 1993–1997 (the 5 years prior to his first stroke) was
rated within normal limits, he required a significantly greater
number of prompts than NCs to recall details of events from
this period, suggesting a subtle deficit in the ability to retrieve
these memories. Not surprisingly, given his very impaired
anterograde memory, SG had even more difficulty recalling
events from his more recent life (largely since his second
stroke). His performance on the recent epoch of the AMI was
rated in the Borderline range. Similarly, when his ability to
recall more detailed autobiographical incidents from the most
recent 5 years was assessed using the mCCT, his performance
was significantly impaired. SG’s wife informed us that on this
measure, all of her husband’s recollections from the last 5
years referred to events that had occurred since his second
stroke (i.e., from the past year). Examination of his responses
from the most recent time period indicated that they were predominately factual with little indication of episodic re-experiencing. For two of the cue words for this time period he
simply responded with “I can’t recall anything”, which in turn
limited the total number of prompts that could be asked.
Anecdotally, compared with his wife’s memory of two
trips in 1999 and 2000 (years between his first and second
strokes), SG’s recollection was quite poor and he had a tendency to confuse events between these two holidays. SG’s
wife stated that he had been able to recollect the events of
these holidays prior to having suffered his second stroke and
reiterated that the first stroke had not resulted in any memory
difficulties that she could detect. Taken together, these findings are indicative of a clear loss of memory for autobiographical incidents from the three (i.e., 1999–2001) years
prior to SG’s second stroke, with more minor difficulties dating back as far as 8 years. More remote autobiographical
events, however, were remembered well.

Semantic memory
Squire and colleagues (Manns, Hopkins, & Squire, 2003;
Reed & Squire, 1998; Squire, 1992; Zola-Morgan, Squire, &

Amaral, 1986) maintain that all types of declarative memories from the time period just prior to lesion onset will be
affected by damage to the hippocampus and adjacent structures. However, there is a growing body of evidence to suggest that retrograde episodic and semantic memories can be
differentially affected (Miller et al., 2001; de Renzi, Liotti, &
Nichelli, 1987; Schacter, Wang, Tulving, & Freedman, 1982;
Tulving et al., 1988; Viskontas, McAndrews, & Moscovitch,
2000, 2002; Warrington & McCarthy, 1988; Yasuda,
Watanabe, & Ono, 1997). Furthermore, differential impairments in semantic knowledge may be evident; Maguire et al.
(2006) reported deficits in knowledge of public events, but
intact recognition of famous faces in a patient with relatively
circumscribed hippocampal damage. As such, we assessed
aspects of SG’s retrograde semantic memory to further investigate the nature of retrograde semantic knowledge subsequent to relatively circumscribed bilateral MTL and
retrosplenial lesions.

Subjects
For all the measures of semantic knowledge, SG’s performance was compared with all 11 NCs as described in
Table 1.

Tasks
The Australian-adapted version of the New Vocabulary test
(Verfaellie, Reiss, & Roth, 1995) was used to assess knowledge of vocabulary that entered the Australian–English
language during the subject’s lifetime. There were ten words
per decade spanning the period 1940–1999. Subjects were
first asked to define each word and where necessary, a threechoice recognition procedure involving possible definitions
was administered. Each item was spoken aloud by the tester
and presented visually. Two scores were recorded for each
decade: the number of definitions correctly recalled and the
number correctly recalled and/or recognised. For both the
recall and recognition conditions, three scores were calculated for each subject. Performance on the ten items from the
subjects’ first full decade of life was taken as the score for
Childhood, the most recent full decade (1990s) was taken as
the score for Recent Life and the Midlife score was an average of the scores achieved for decades between the first
decade and 1990.
Each subject’s knowledge of famous faces and public
events was also assessed using Shum and O’Gorman’s (2001)
Australian Remote Memory Battery. The Famous Faces subtest utilized black and white photographs of famous people’s
faces. These were shown one at a time to the subject, who
was then asked to recall the person’s name. Half points were
awarded for providing only the first or last name (in such
cases, the subject was prompted for the full name). A three
choice recognition procedure, using three famous names as
possible options, followed for incorrect items. The Public

RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS
Table 5. SG’s performance on tests of semantic knowledge
SG’s Score

NC mean (sd)

t

p

9.6 (0.6)
9.4 (0.5)
7.5 (1.9)

0.63
0.05
1.29

0.271
0.480
0.113

New Vocabulary1 Recognition (/10)
Childhood
10
10 (0.01)
Midlife
10
9.9 (0.2)
Recent Life
10
9.5 (0.5)

0
0.40
0.83

0.5
0.348
0.212

Famous Faces2 Recall (/9)
Childhood
2
Midlife
4.5
Recent Life
5

3.8 (1.2)
4.7 (2.1)
5.5 (2.1)

−1.45
−0.08
−0.21

0.089
0.469
0.419

Famous Faces2 Recognition (/9)
Childhood
8
Midlife
8.25
Recent Life
8

6.8 (1.3)
8.4 (0.5)
8.9 (0.3)

0.85
−0.24
−2.89

0.207
0.408
0.008

Public Events2 Recall (/9)
Childhood
2.5*
Midlife
6.13
Recent Life
6

7.9 (1.1)
7.5 (0.8)
7.6 (1.1)

−4.56
−1.62
−1.40

0.001
0.068
0.096

Public Events2 Recognition (/9)
Childhood
6*
Midlife
7.75*
Recent Life
9

8.8 (0.4)
8.9 (0.2)
8.9 (0.2)

−6.67
−7.21
0.56

0.000
0.000
0.317

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New Vocabulary1 Recall (/10)
Childhood
10
Midlife
9.38
Recent Life
10

*=significantly different from the control group, based on calculations performed using Crawford & Garthwaite’s (2001) programme ‘singlims’ and
sequentially rejective Bonferroni corrections (Holm, 1979).

Events subtest was used to assess memory for past news
events. Questions pertaining to famous events were administered simultaneously in oral and written form and a free recall
format was used initially followed by a three choice recognition procedure for any incorrect items. For both subtests,
there were nine items per decade. Only decades relevant to
each subject’s lifetime were used in this study. Results for the
Famous Faces and Public Events subtests were analysed in
the same manner as outlined for the New Vocabulary test.
That is, for both the recall and recognition conditions, three
scores were calculated for each subject (Childhood, Midlife
and 1990s).
Results
There were no differences detected between SG and the NCs
on the New Vocabulary test or Famous Faces subtest, for
either recall or recognition for any of the three time periods
examined (Table 5). On the Public Events subtest, SG’s performance on the Childhood (p < .013) epoch for recall and on
the Childhood (p < .008) and Midlife (p < .008) time periods
for recognition was impaired relative to NCs (see Table 5).

109

His scores did not differ from control subjects when asked
questions about public events from the 1990s.
Comment
SG’s performance was comparable to NCs on both the recall
and recognition conditions of the New Vocabulary test
(Miller & Batchelor, 2004; Verfaellie et al., 1995) and there
was no evidence of a temporal gradient. However, it was
noted that the NC group and SG performed at ceiling on this
test, which raised the possibility that any subtle impairments
in knowledge of vocabulary terms may have been obscured.
On the Famous Faces test, where there was sufficient variation in the NC data, SG’s performance was well within normal limits across all time periods tested. Other aspects of
semantic knowledge (as shown earlier in Table 1) also indicated intact abilities; semantic fluency, picture naming, word
definition and word-picture matching scores as well as his
scores on the WAIS-R Information and Vocabulary subtests
all fell at or above the average range.
In contrast, SG’s memory for public events from most
periods of his life was deficient. Although the current study
did not control for the effects of possible differences in media
exposure, which has been shown to influence performance on
tests of retrograde semantic knowledge (Kapur et al., 1999),
this explanation is unlikely to account for SG’s poor memory
for remote public events for three reasons (1) the control
group was matched to SG in terms of level of education and
intellectual function, (2) premorbidly, SG was a high functioning and well travelled individual who (according to his
wife) regularly listened to the news and read newspapers, and
(3) SG’s performance was comparable to the NC group on all
aspects of the Famous Faces test. Surprisingly, he did not
show a significant deficit in memory for public events from
the 1990s. Unfortunately, inspection of the public events data
from this decade again revealed a possible ceiling effect, particularly for the recognition component.

Discussion
Detailed investigations into SG’s memory for the past indicate that some, but not all aspects of retrograde memory are
dependent on mesial temporal and/or retrosplenial brain
regions. SG’s impaired ability to identify photographs of
landmarks from both the remote and recent time periods indicated that the mesial temporal lobes and/or retrosplenial cortices are involved in the processing of this type of
information indefinitely. He was also unable to determine the
direction of one landmark in relation to his position in front
of another landmark. A temporal gradient was seen for autobiographical event memory; SG’s recall of autobiographical
event memories from the few years prior to his strokes was
deficient, whereas his recall of autobiographical incidents
from the more remote past was intact. In contrast, his

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I.J. HEPNER ET AL.

memory for public events seemed to be impaired for much of
his lifetime. Knowledge of routes, cardinal direction, landmark locations, personal semantic details, vocabulary and
famous faces were all preserved.

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Topographical memory
With regard to his retrograde topographical memory deficits,
SG encountered difficulty when he was required to identify
major or incidental landmarks across all time periods tested
Aguirre and D’Esposito (1999) and others (e.g., Epstein &
Kanwisher, 1998; Habib & Sirigu, 1987; Rosenbaum, Gao,
Richards, Black, & Moscovitch, 2005) would attribute such
landmark agnosia to a loss of posterior parahippocampal/
anterior lingual gyrus function. These findings only offer partial support to the notion proposed by Rosenbaum et al.
(2000), who argue that bilateral mesial temporal lobe damage
results in a loss of detailed topographical information. Given
the findings from SG, it is perhaps more appropriate to conclude that damage to the posterior parahippocampal/anterior
lingual gyri (as sustained by both SG and KC) results in a
temporally extensive recognition deficit for landmarks per se.
This notion complements the findings of Maguire et al.
(2006) who documented intact landmark recognition in their
patient TT, with relatively preserved parahippocampal gyri in
the context of focal hippocampal damage. A role for the right
posterior parahippocampal gyrus in the identification of
familiar landmarks has been documented in two functional
neuroimaging studies (Rosenbaum et al., 2004b; Rosenbaum,
Ziegler, Winocur, Grady, & Moscovitch, 2004c). Both these
studies examined their subjects’ topographical memories for
their current home town only. To our knowledge, there have
not been any functional neuroimaging studies to date that
have investigated recognition or identification of landmarks
that were encountered in the remote past. Findings from the
current study indicate that the posterior parahippocampal/
anterior lingual gyri may be the permanent repository for
knowledge pertaining to landmark identity, and as such, we
predict that there would be posterior parahippocampal/anterior lingual involvement in landmark identification, regardless of the age of the memory.
A second topographical memory deficit that we detected in
SG was his heading disorientation. That is, he was poor at
imagining which direction he would have to turn his body to
move from one landmark to another. Through his intact performance on the cardinal direction subtest, SG demonstrated
that he was able to imagine himself standing in a particular
position relative to a given landmark. Neither he nor his wife
described any classic signs of egocentric disorientation (as
outlined by Aguirre and D’Esposito, 1999) and he performed
normally on table top tests of visuospatial ability This would
suggest that SG’s difficulties in judging the spatial relationships between landmarks based on his imagined position
were either the result of problems with allocentric processes
or with transforming spatial information from an egocentric

to allocentric frame of reference. His intact performance on
the landmark map localisation and route recall subtests,
which both require some form of allocentric processing,
make this first explanation less likely. A number of researchers have theorised that the retrosplenial cortex may be instrumental in performing spatial transformations because of its
connections with the posterior parietal lobe and parahippocampal gyrus (Maguire, Frith, Burgess, Donnett, & O’Keefe,
1998; Vogt, Finch, & Olson, 1992). This notion is particularly significant since neither EP, KC or TT (who were unimpaired on similar tasks) sustained bilateral retrosplenial
damage, whereas FDG-PET and MRI data indicated that SG
had. Patients with damage to the retrosplenial cortices have
been described by Aguirre and D’Esposito (1999) as suffering from heading disorientation: an inability to derive directional information from landmarks that they are able to
recognise. It is therefore quite plausible that SG was unable to
derive directional information even from landmarks, because
he had difficulty transforming spatial information from an
egocentric to an allocentric representation (and vice versa).
Interestingly, our findings indicate that damage to the retrosplenial regions does not necessarily affect one’s appreciation for cardinal direction. Compared to making spatial
relationships judgements, identifying cardinal direction relied
on the application of well established knowledge regarding
Sydney, which subjects were heard to verbalise as they performed the test. For example, knowing that the “North
Shore” lies at the far end of the Sydney Harbour Bridge
allowed subjects to deduce the north–south axis of the city.
Future studies, using healthy subjects and patients with circumscribed retrosplenial damage are warranted to further
investigate the neural mechanisms underlying the appreciation of cardinal direction and the cognitive processes used by
normal subjects to determine cardinal direction.
Despite his virtually complete bilateral hippocampal damage, SG retained some form of spatial map that allowed him
to access information regarding routes and positions of landmarks within a familiar environment. Both Teng and Squire
(1999) and Rosenbaum et al. (2000) also reported that their
subjects (both with almost complete damage to both hippocampi) were able to recall such information. These findings
contrast somewhat with those of Maguire et al. (2006), who
documented poor navigational ability in areas that did not
contain many (or any) major roads. Methodological differences may account for this discrepancy, as Maguire et al.’s
patient TT was asked to navigate in a virtual reality environment, whereas SG, EP and KC were asked to recall routes
from memory. Furthermore, none of the three latter subjects
were required to navigate in areas that did not contain any
major roads. Thus, more subtle deficits in route knowledge
may have been missed.
Taken together, it would appear that the hippocampi are
not necessary to support memory for most aspects of remotely
learned topographical information, contrary to the predictions
of Cognitive Map Theory (O’Keefe & Nadel, 1978). More
recently, it has been proposed that the hippocampus might

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RETROGRADE MEMORY SUBSEQUENT TO BILATERAL MTL LESIONS
only be necessary for the initial acquisition and navigation
within novel environments and that the right caudate nucleus,
lateral temporal or posterior parietal cortices are essential for
the maintenance of these long-term topographical memories
(Aguirre & D’Esposito, 1999; Hartley, Maguire, Spiers, &
Burgess, 2003; Rosenbaum et al., 2004b,c). In support of
this, in another study (manuscript in preparation), we have
documented poor route recall in patients with combined temporal and parietal atrophy. In combination with these and previous results, findings from SG suggest that the posterior
parietal cortices alone are sufficient for storing this sort of
material. Nonetheless, the fact that TT had difficulty with
memory for lesser routes (and that KC had difficulty recognising less obvious landmarks in his neighbourhood) continue
to raise the possibility that the hippocampi do play a role in
the very long-term storage of the fine details of topographical
knowledge.

Autobiographical memory
The results of autobiographical event memory testing in SG
were more consistent with Consolidation Theory than MTT,
as SG had a deficit for recent autobiographical events, but
was able to recall detailed autobiographical events from the
more distant past. Our findings do not support the notion that
remote autobiographical memories are less vivid or recalled
in less detail after mesial temporal lesions (Fujii et al., 2000;
Gilboa, Winocur, Grady, Hevenor, & Moscovitch, 2004). It
seems possible that KC’s inability to recall any detailed autobiographical incidents may be attributable to the widespread
nature of his brain lesions, which has resulted in additional
deficits (such as adynamia and reduced verbal generativity)
that have compromised his capacity for complex and effortful
retrieval. For example, KC has been described as someone
who “does not initiate any optional activity on his own, has
difficulty planning complex actions and … when asked to
describe the state of his mind when he is trying to think about
any part of his past or future, he says that it is blank” (Tulving
et al., 1988, pp. 7–8).
However, subject TT, with a more circumscribed temporal lobe lesion was also unable to recall any autobiographical incidents from any point in his life (Maguire et al.,
2006). Cipolotti and colleagues (Cipolotti et al., 2001)
reported similar findings in a patient with markedly
shrunken hippocampi. Interestingly, both these patients suffered from several seizures during the course of their recovery, which may have served to disrupt or interfere with
processes vital to the long-term storage of autobiographical
incidents (Lah, Grayson, Lee, & Miller, 2004). Of note, neither SG, EP nor any of the patients with MTL lesions studied by Bayley, Hopkins, and Squire (2003), who all had
good recollection of remote autobiographical events, were
reported to have experienced seizures. Hence, in addition to
demonstrable neuroanatomical variables (i.e., lesion locus),
factors such as whether or not the subject experienced

111

seizures may play an important role in determining the
pattern of autobiographical memory loss.
Of note, the degree of autobiographical memory loss
observed in SG was not as extensive as that documented in
EP (Reed & Squire, 1998). Differences in locus of lesion
probably explain this discrepancy. SG’s lesion involved primarily the mesial temporal lobes and retrosplenial cortices,
with sparing of the anterior lateral inferotemporal cortex.
EP’s damage primarily affected anterior mesial temporal
structures and extended to include the lateral inferotemporal
gyri (Hamann & Squire, 1997), which are thought to be particularly important with regard to the processing of remote
autobiographical event memories (Calabrese et al., 1996;
Fink et al., 1996; Markowitsch et al., 1993).
In patients with posterior brain lesions, a number of
researchers have proposed an association between an ability
to generate mental imagery and the successful recollection of
autobiographical incidents (Hunkin et al., 1995; O’Connor,
Butters, Miliotis, Eslinger, & Cermak, 1992; Ogden, 1993;
Rubin & Greenberg, 1998). Furthermore, a loss of memory
for autobiographical incidents across the entire lifespan has
been documented in a patient with retrosplenial tumour
(Gainotti, Almonti, Di Betta, & Silveri, 1998). Surprisingly,
in spite of his bilateral retrosplenial lesions, SG demonstrated
a limited loss of memory for autobiographical episodes.
However, his lesions were more restricted in nature than the
patients described by Gainotti et al. (1998) and the cases
reviewed by Rubin and Greenberg (1998). Furthermore, he
showed no loss of visual imagery (as demonstrated by normal
performance on mental imagery control tasks). Taken
together, it appears that mesial parietal and occipital regions
outside the retrosplenial cortex have an important role in the
processing of autobiographical memories, most likely
through the formation of mental images.

Semantic memory
SG demonstrated relatively preserved performance on tests of
memory of personal semantic details, vocabulary, object
naming, famous people naming and semantic fluency. This
contrasts somewhat with KC’s pattern of performance on
tests of famous names and vocabulary knowledge, where he
showed a dense loss of information that had been acquired
during the 5 years prior to his injury, but preserved ability on
all other time periods examined (Westmacott & Moscovitch,
2002). Although SG did not show a similar loss of recently
acquired information, it is possible that this difference might
be accounted for in terms of methodology. Specifically, KC’s
knowledge was tested for information encoded in 5-year
intervals, while SG’s memory was examined for information
that had been prominent during each full decade from 1940 to
2000. If SG does indeed have a subtle and very temporally
limited deficit for this sort of information, our tests may not
have been able to detect it. As such, it is not possible to rule
out that SG may have a very restricted retrograde amnesia for

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I.J. HEPNER ET AL.

famous faces or vocabulary terms, as might have been predicted by both Consolidation Theory and MTT. TT may also
show a very restricted retrograde amnesia for famous faces,
as Maguire et al. (2006) comment that his only errors on
famous face recognition were for faces that had come to
prominence 3 years prior to testing (i.e., his impairment may
extend to include the year prior to his illness).
Nevertheless, neither SG, KC nor TT showed an extensive
loss of knowledge for vocabulary and famous people, as documented for subject EP. This discrepancy is again considered
attributable to differences in the locus of the subjects’ lesions.
The inferior and anterolateral temporal cortices have been
implicated in the long-term processing of knowledge regarding objects and vocabulary (e.g., Hodges, Patterson, Oxbury,
& Funnell, 1992; Kitchener, Hodges, & McCarthy, 1998;
Verfaellie et al., 1995) and a role for fusiform gyrus in the
identification of famous faces has been proposed (GornoTempini & Price, 2001; Haxby et al., 1994). These areas are
largely spared in SG, KC and TT but damaged in EP. Hence,
memory for remotely learned vocabulary and famous faces
may not be dependent on mesial temporal lobe function at all
but rather would seem to be processed by anterior temporal
and fusiform cortices, respectively.
Given temporally limited deficits or intact performance
found on other aspects of semantic memory, SG’s subtle but
temporally extensive deficit on a test of public event memory
was somewhat surprising. However, both TT and EP also
demonstrated poor knowledge of public events (and KC’s
knowledge for this material was not tested). Previous studies
of patients with bilateral damage limited to the hippocampal
formation have demonstrated a time-limited loss of knowledge regarding public events (e.g., Hirano & Noguchi, 1998;
Kapur & Brooks, 1999), while studies of patients with more
extensive temporal lobe cortical damage (e.g., Cermak &
O’Conner, 1983; Damasio, Eslinger, Damasio, VanHoesen,
& Cornell, 1985; Kapur et al., 1996) and patients with temporal lobe epilepsy (Lah, Lee, Grayson, & Miller, 2006) have
revealed more pervasive losses of memory for public events.
A more complete understanding of the neural representation
of public event memory would seem to depend on the accumulation of more cases with temporal lobe lesions who are
tested and compared to appropriate control subjects.
In conclusion, the current findings indicate that retrograde
topographical, autobiographical and semantic memories can
be differentially affected subsequent to bilateral mesial temporal and/or retrosplenial damage caused by infarction. It
seems clear that the site and extent of a temporal lobe lesion
influences the pattern of retrograde memory deficits. None of
the existing theories (Cognitive Map, Consolidation or Multiple Trace) accounted for all the findings adequately, although
many of the predictions of Aguirre and D’Esposito (1999)
regarding topographical memory were corroborated. Considering our findings in the context of the existing literature, we
concur that posterior parahippocampal damage affects landmark recognition and identification and that retrosplenial
lesions interfere with spatial transformations (egocentric to

allocentric representations). Hence, a lesion to one of these
two areas would be expected to affect one’s memories for
these particular types of information, irrespective of how
long ago they were first acquired. On the other hand, these
two brain regions have little role to play in other aspects of
retrograde topographical memory such as memory for spatial
maps and knowledge of cardinal direction. It is possible that
these functions rely on posterior parietal or temporal cortices.
SG’s results also indicate that the mesial temporal lobes and
retrosplenial region have a time-limited role in the processing
of retrograde autobiographical events and no role in the retention of personal semantic details. The temporally extensive
deficit for public events seen in SG and in some other
patients with relatively selective MTL lesions fits with neither MTT or Consolidation Theory and merits further investigation. Knowledge pertaining to famous faces, vocabulary
and objects may depend temporarily on the MTL, but SG’s
results in the context of the literature suggest that these sorts
of semantic memories depend more on inferior temporal cortex lateral or anterior to the parahippocampal gyrus and rhinal
cortices.
Original manuscript received 13 June 2006
Revised manuscript accepted 16 March 2007
First published online 19 May 2007

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