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The Journal of Neuroscience, August 1, 2000, 20(15):5853-5857
Remote Episodic Memory Deficits in Patients with Unilateral
Temporal Lobe Epilepsy and Excisions
Indre V.
Viskontas1,
Mary Pat
McAndrews1, 2, and
Morris
Moscovitch1
1 Department of Psychology, University of Toronto, and
2 Neuroscience Program, University Health Network, Toronto
Western Hospital, Toronto, Ontario M5T 2S8, Canada
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ABSTRACT |
The nature of remote memory impairment in patients with medial
temporal lobe damage is the subject of some debate. While some investigators have found that retrograde amnesia in such patients is
temporally graded, with relative sparing of remote memories (Squire and
Alvarez, 1995 ), others contend that impairment is of very long duration
and that remote memories are not necessarily spared (Sanders and
Warrington, 1971; Nadel and Moscovitch, 1997). In this study, remote
memory was assessed in 25 patients with unilateral temporal lobe
epilepsy and 22 non-neurologically impaired controls using the
Autobiographical Memory Interview (Kopelman et al., 1989).
Results indicate that patients have impaired personal episodic memory
but intact personal semantic memory. The impairment extends even to the
most remote time periods in early childhood, long before seizure onset
in many patients. As well, patients awaiting temporal lobectomy for
control of seizures perform as poorly as those who have already
undergone resective surgery. These results support the hypothesis that
temporal lobe damage or dysfunction, caused by recurrent seizures or
surgical excision, results in extensive retrograde amnesia for personal
episodic memories. Interestingly, patients with radiological evidence
of hippocampal sclerosis were not significantly more impaired than those without obvious sclerosis. These results indicate that even minimal damage to medial temporal lobes results in significant impairment to autobiographical episodic memory. These findings are more
compatible with a memory loss or retrieval deficit rather than a
consolidation account of remote memory impairment.
Key words:
remote memory; episodic memory; epilepsy; temporal
gradient; multiple trace theory; consolidation; autobiographical
memory
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INTRODUCTION |
The study of remote memory is key to
understanding the role of the hippocampal complex in memory
consolidation. The development of a standardized test, the
Autobiographical Memory Interview (AMI), by Kopelman et al. (1989,
1999) has made it easier to assess personal remote memory reliably in
humans. The AMI measures personal semantic and episodic memories from
different time periods childhood, early adulthood, and the recent
pastpermitting examination of the possible differential effects of
brain damage on these two types of autobiographical memory.
In keeping with earlier observations (Ribot, 1882; Burnham, 1903;
Scoville and Milner, 1957) Squire (1992) and Squire and Alvarez (1995)
noted a temporal gradient to retrograde amnesia (RA) associated
with medial temporal damage with the most remote memories
differentially spared. He concluded that the hippocampus is involved in
the establishment of new memories and their temporary storage but that
over time these memories become independent of the hippocampus through
consolidation. Once consolidation is complete, the memory trace resides
elsewhere, rendering the hippocampus unnecessary for retrieval.
According to consolidation theory, patients with temporal lobe epilepsy
(TLE) and damage to the hippocampal system, should show a temporal
gradient on remote memory tests. Furthermore, damage to this region
should have a similar effect on all forms of declarative memory with no
distinction among episodic and semantic memories, assuming no
differential rehearsal.
Nadel and Moscovitch (1997) describe an alternative theory of
hippocampal function called the multiple trace theory (MTT). According
to MTT, the hippocampal complex rapidly binds novel information and
experience into a coherent memory trace composed of the hippocampal
elements active at the time of encoding and the neocortical (or other)
neurons that represent the events' features or components. Each
episodic (autobiographical) memory trace consists of this ensemble of
neurons as long as it exists. No long-term consolidation process is
postulated in which the hippocampal contribution is relinquished. The
reactivation of a memory trace establishes a new representation that
shares some or all of the information in the original trace. The
creation of multiple episodic traces lays down an associative network
of related information and initiates the formation of semantic memory stores. These stores are based on extracts of factual information from
the episodes and can be coded independently from them. Because MTT
postulates that the hippocampal complex is an integral part of the
autobiographical memory as long as it exists, damage should lead to
loss of even remote episodic memories.
According to this account, the probability of recalling a remote event
depends on the number of traces that code relevant information. Because
it is unlikely that autobiographical episodes will be recovered in full
detail, fewer complete traces will be laid down for them than for
personal semantic information. As a result, after hippocampal complex
lesions, the temporal gradient is expected to be shallower and extend
back further in time for autobiographical episodes than for semantic
memories. Our study set out to test the contrasting predictions made by
these theories regarding loss of episodic and semantic memory after
medial temporal lobe damage.
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MATERIALS AND METHODS |
Participants
Twenty-five patients with TLE participated in the study. Eleven
patients had seizures originating in the right temporal lobe, five of
whom were being assessed for resective surgery, and six of whom had
already undergone surgery. Fourteen patients had seizures originating
in the left temporal lobe, eight of whom were being assessed for
surgery, and six of whom had already undergone surgery. All patients
had documented damage involving the medial temporal region. In the
preoperative group, there was 1 case with tumor, 2 with cavernomas, and
10 with radiological evidence of mesial temporal sclerosis. Cases with
surgical resections involved excision of the amygdala and 1-2 cm of
hippocampus. Three patients had pathology in additional areas
independent of their seizure focus; one with a small region of
encephalomalacia in the left occipital pole, one with atrophy of the
right thalamus, and one with cavernomas in the left thalamus/insula.
All patients that had undergone surgery were either seizure-free
postoperatively or had a 75% reduction in seizure frequency. Those
tested postoperatively were seen at least 5 months and at most 8 months
after surgery.
Twenty-two non-neurologically impaired controls matched for age and
education also participated. All participants gave informed consent,
and controls were paid $20.00 each for their participation. Control
participants had no history of epilepsy or other neurological disease
and were recruited using advertisements in the hospital, whereas
patients were asked if they would like to participate by the
neuropsychologist conducting their clinical assessment. Patients and
controls were all right-handed, with the exception of one control (LS).
There were 12 female and 13 male patients and 11 female and 11 male controls.
Demographic information for participants is presented in Table
1; patient and control groups were
matched for age and years of education. Table
2 displays relevant psychometric data for patients, including full-scale intelligence quotient (Weschler Adult Intelligence Scale-Revised or Weschler Adult Intelligence Scale-III) and standardized scores (z scores)
representing delayed recall from WMS measures of paragraph
recall and visual reproduction. The latter measures were selected to
characterize anterograde memory functioning in our patient sample.
Because different versions of the Weschler Memory Scale (WMS-R and
WMS-III) were used across patients, z scores were calculated
based on normative reference data provided in test manuals. The
proportion of patients who had mesial temporal sclerosis by
radiological criteria and the mean age of seizure onset are also
displayed in Table 2.
Materials and design
Administration and scoring procedures as described in the AMI
test manual (Kopelman et al., 1989) were followed. The interview consists of two types of questions, administered concurrently: (1)
personal semantic questions, and (2) autobiographical incidents questions. The questions survey three distinct time periods: childhood (ages 0-18), early adulthood (ages 18-30), and recent (within the
past 5 years). As well, the early time period can be further subdivided
into three time periods: ages 0-5, ages 5-11, and ages 11-18.
Personal semantic questions. Subjects were asked questions
relating to their personal past, including names and locations of
schools attended, home addresses, and names of friends. Each time
period had a maximum score of 21 points.
Autobiographical incidents questions. Subjects were asked to
relate incidents that occurred during each of the three time periods
and to give temporal and spatial contextual information for each
incident described. Three such incidents were probed for each time
period, and specifications such as "first day at work" were used as
probes. Responses were recorded on the scoring sheets as close to
verbatim as possible. Each incident was scored out of a possible score
of 3, based on the descriptive richness and specificity in time and
place of the response. The maximum score per time period was 9. One
rater scored each of the questions, and an independent rater who was
blind to subject group and original ratings scored 25% of the episodic items.
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RESULTS |
Participants
There were no significant differences between groups for age or
education (p > 0.05). TLE patients demonstrated
mild memory deficits on the WMS, with left TLE patients showing
selective verbal recall impairment, whereas right TLE patients had
equivalent difficulty with both verbal and nonverbal recall. A 2 (hemisphere) × 2 (preoperative vs postoperative status) × 2 (material) ANOVA revealed a significant side by material interaction
(F(1,20) = 7.575; p < 0.02). Of note, there was no main effect or interaction involving
operative status, indicating that those patients awaiting surgery
showed equivalent anterograde memory impairments to those who had
undergone temporal excisions.
AMI
Figures 1 and
2 display the mean scores for personal
semantic and episodic questions by time period for patients and
controls. Note that the two test components are on different scales
because the total possible score for semantic questions is 21 and for episodic items is 9 for each time period.
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Figure 1.
Personal semantic memory performance. Mean scores
on semantic components of AMI for control (n = 22)
and patient (n = 25) groups. The maximum score is
21 per time period. Vertical lines depict SEM
values.
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Figure 2.
Autobiographical episodic memory performance. Mean
scores on episodic components of AMI for control (n = 22) and patient (n = 25) groups. The maximum
score is 9 per time period. Vertical lines depict SEM
values.
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Inter-rater reliability
An interclass correlation (Howell, 1997) was used to evaluate
inter-rater reliability for responses scored by two individuals. The
resulting coefficient was 0.75, which compares favorably with those
reported in the test manual (0.83-0.86).
Overall ANOVA
Proportions were used to compare episodic and semantic data,
because these are based on different numbers of total points. An
arcsine transformation was performed before analysis to ensure homogeneity of variances. A 2 (group) × 3 (time) × 2 (type)
ANOVA revealed a main effect of group
(F(1,45) = 55.81; p < 0.001), with patients performing significantly more poorly than
controls. There was also a main effect of type
(F(1,45) = 57. 74; p < 0.001) and a significant type by group interaction
(F(1,45) = 47.38; p < 0.001). As shown in Figures 1 and 2, differences between patients and
controls were confined to the episodic questions. There was a
significant main effect of time (early, middle, and recent) (F(2,90) = 6.90; p < 0.002), with better performance for more recent periods. None of the
interactions involving time was significant.
Separate analysis of the semantic items showed no significant effect of
group (F(1,45) = 0.885;
p = 0.352). There was a significant effect of time
(F(2,90) = 6.69; p = 0.002), but no time × group interaction
(F(2,90) = 0.370; p = 0.692). For the episodic section, significant effects were observed for
group (F(1,45) = 78.15; p < 0.001) and time
(F(2,90) = 3.23; p < 0.04), but the interaction was not significant
(F(2,90) = 0.971; p = 0.382).
Additional analyses
Performance on the episodic component was evaluated further in the
patient group to ascertain whether there were significant differences
according to clinical variables, including age of onset of epilepsy,
preoperative versus postoperative status, presence of medial temporal
sclerosis by MRI, and affected hemisphere. None of these analyses
revealed any significant main effects or interactions (with time
period). Given the nature of the patient population, in which age of
onset of epilepsy ranged from 0 to 36 years, it was also possible to
examine recall of episodes occurring before and after the onset of
recurrent seizures using the three earliest time periods (0-5, 5-11,
and 11-18 years) from the AMI. Eight patients had seizures beginning
before age 5 (mean age of onset, 3.5), and 11 patients had recurrent
seizures beginning after age 18 (mean age of onset, 24.5 years). There
was no significant differences
(F(1,17) = 2.78; p > 0.11) in recall scores for autobiographical episodes across time
periods for these two patient subgroups and no significant interactions
with time (Fig. 3).
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Figure 3.
Autobiographical episodic memory performance
during earliest time periods. Mean scores on episodic components of AMI
for control (n = 22), late seizure onset
(n = 11), and early seizure onset
(n = 8). Late seizure onset describes patients who
reported first seizures after age 18, early seizure onset describes
patients who reported first seizures before age 5. The maximum score is
3 per time period.
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DISCUSSION |
There are three key features of our finding of remote memory
impairment in patients with temporal lobe epilepsy: defective retrieval
of episodic memories with sparing of personal semantic memories, lack
of a temporal gradient to the episodic memory deficit, and a duration
that extended to early childhood. These results are consistent with the
MTT of Nadel and Moscovitch (1997) but difficult to reconcile with
consolidation theory (Scoville and Milner, 1957; Squire and Alvarez,
1995).
Our TLE patients exhibited no difficulties with recall of personal
semantic memories despite profound impairment in recall of
autobiographical episodes. Indeed, both patients and controls could
recall semantic information readily even for the most recent time
periods, indicating that such information is accessed easily. MTT
suggests that personal semantic memories are more resistant to
hippocampal damage because of multiple traces established through many
retrieval attempts in the past and/or the evolution of independent semantic traces via the same mechanism. In contrast, consolidation theory proposes that hippocampal damage should affect episodic and
semantic memories similarly, unless differential rehearsal can account
for the relative sparing of semantic memories. Of course, this "add
on" to consolidation theory regarding differential rehearsal is one
of the processes by which MTT suggests semantic memories become
resistant to disruption (for further discussion, see Moscovitch and
Nadel, 1998, 1999; Nadel and Moscovitch, 1998).
There was no evidence of a temporal gradient in remote memory loss for
personal episodes, with both patients and controls demonstrating better
retrieval of more recent memories relative to more remote ones. The
absence of a temporal gradient is not compatible with consolidation
theory, which is founded on the principle of differential sparing of
remote memories. However, this pattern can be accommodated by MTT if
one assumes that episodic memories are not multiply reproduced in all
their detail. Although the gist of the episode may be reproduced, the
complete episode will leave few traces, and thus retrieval remains
dependent on the hippocampal complex, which includes the hippocampal
formation and perihippocampal structures (parahipocampal, perirhinal,
and entorhinal cortex). Conceivably, our patients were attempting to
retrieve unique experiences that had not been subject to many previous
retrieval attempts from each time period, and thus no temporal gradient
would be expected.
Review of the literature on retrograde amnesia indicates that the
existence of a temporal gradient and its length depends on the extent
of damage to the hippocampal complex; the greater the damage, the more
severe and extensive the retrograde loss (Nadel and Moscovitch, 1997;
Fujii et al., 2000). According to MTT, partial damage to this
region results in temporally graded RA, because the multiple traces for
more remote memories make them more resistant to loss. Complete damage
results in loss of all episodic memories and an inability to retrieve
more "vulnerable" semantic information that had been weakly
encoded. This general pattern is also demonstrated in the RA of
patients described by Squire and his colleagues (McKinnon and Squire,
1989; Rempel-Clower et al., 1996; Reed and Squire, 1998). Lesions
restricted to the hippocampus proper result in minimal RA, whereas more
extensive lesions produce an RA for a decade or more before injury,
with complete hippocampal complex lesions leading to complete loss of
episodic memories. Of interest, our data do not reveal any association
between the measures we used to assess the degree of medial temporal
damage/dysfunction and the extent of remote memory impairment. The
measures of hippocampal damage included age of onset (an indirect
measure) and presence of hippocampal sclerosis (a direct measure).
Alternatively, it is conceivable that damage to other temporal lobe
structures, such as the temporal pole (Markowitsch, 1995) is crucial in
producing extensive RA. This is an unlikely explanation for our data,
because there was no difference between postoperative patients, all of
whom had the temporal pole resected, and those still awaiting surgery,
whose temporal pole was presumed to be intact. We cannot discount the
possibility, however, that seizure activity may have affected the
temporal pole in all patients and reduced its function. Similarly,
whereas damage or dysfunction in other temporal neocortical regions
cannot be ruled out in our patients, the common region affected is the
hippocampal complex.
To our knowledge, no studies have been published that report
performance by TLE patients on the AMI, although similar findings of
relative impairment on the episodic component have been described in a
small sample of postoperative patients (O'Connor et al., 1999).
Kopelman et al. (1989) reported that amnesic participants were impaired
on both semantic and episodic portions of the test and that they showed
a shallow temporal gradient, with partial sparing of more remote
memories. Of interest, they found that age influenced the slope of the
gradient, with young amnesics (age, <40 years) showing a relatively
flat gradient and older amnesics (age, >50) demonstrating a more
marked gradient. We note that the majority of our TLE patients were
under age 50. In a recent study, Kopelman et al. (1999) reported a
relatively flat temporal gradient for the recall of both personal
semantic facts and autobiographical incidents by herpes encephalitis
patients with extensive bilateral damage to the temporal lobes.
However, as Kapur (1999) argued in his extensive review of retrograde
amnesia, there are a number of studies documenting dissociations
between episodic remote memories and related personal semantic
memories. Because unilateral TLE patients in our study do not show
impairment on the personal semantic questions, it may be argued that
semantic memories are dually represented in both hemispheres and that
bilateral damage is necessary to show such impairment. For episodic
memories, however, different aspects may be represented in each
hemisphere, making them more vulnerable to loss in the event of
unilateral damage. This hypothesis may explain why patients can recall
some episodic memories from a specific time period but not others.
It should be noted that the results reported in this study do not
replicate those reported in a similar study by Barr et al. (1990). They
examined patients who had undergone unilateral temporal resections for
epilepsy on an extensive battery of remote memory tests, one of which
is described as an "exhaustive array of questions concerning various
life events and circumstances" that appears to tap similar episodic
and semantic personal memories as the AMI. They found that only left
TLE patients showed remote autobiographical memory impairments, whereas
we found that both left and right TLE patients were impaired. A number
of reasons can account for this discrepancy, among them, differences in
the types of remote memory tests used as well as possible differences
in the extent of lesions to the right and left temporal lobes.
One concern in assessing remote memory in patients with epilepsy is the
difficulty in precisely dating the onset of the critical damage and
thus providing an unequivocal temporal landmark for retrograde amnesia.
Clearly, using the time of excision as this landmark is inadequate.
Significant hippocampal damage is found in many patients with TLE
before resective surgery (Miller et al., 1993), and the removal of a
nonfunctional hippocampus may not produce any additional anterograde
memory defect (Hermann et al., 1994). Our analysis of the episodic
memory data according to age of onset of epilepsy speaks to this issue.
We found the same extent and pattern of memory loss in the earliest
time periods (ages 0-18) for patients whose seizures began before age
five and those whose seizures began after age 18. This finding suggests that the impairment in patients with late onset and likely those with
early onset is retrograde in nature. Although the possibility of
defective encoding in both groups cannot be discounted (i.e., even
those with later onset may have had damaged medial temporal tissue
before experiencing recurrent seizures), the absence of even a trend in
the data for poorer performance by the early onset group weakens this conclusion.
In summary, findings from this study have helped to characterize remote
memory in patients with temporal lobe epilepsy. Patients with
unilateral temporal lobe pathology show greater loss of episodic than
semantic autobiographical memories, as measured by the Kopelman AMI.
Furthermore, this loss encompasses all time periods equally, extending
even to early childhood. Findings from this study are generally
consistent with the multiple trace theory of hippocampal function in
memory and incompatible with the predictions of consolidation theory.
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FOOTNOTES |
Received Dec. 22, 1999; revised May 5, 2000; accepted May 9, 2000.
This work was supported by Grant A8347 from the Natural Sciences and
Engineering Research Council of Canada (M.M.) and by the Clinical
Neuroscience Research Fund of the University Health Network (M.P.M.).
For their contribution and time, we thank the patients and control
participants. We also thank Stephen Taylor for help with the
statistical analysis and Mary Jaciw for assistance in compiling
psychometric data and scoring for analysis of inter-rater reliability.
This research was completed in partial fulfillment of requirements for
an undergraduate thesis at the University of Toronto.
Correspondence should be addressed to Mary Pat McAndrews, Neuroscience
Program, EC2-009, Toronto Western Hospital, 399 Bathurst Street,
Toronto, Ontario M5T 2S8, Canada. E-mail: mcandrws{at}uhnres.utoronto.ca.
| |
REFERENCES |
-
Barr WB,
Goldberg E,
Wasserstein J,
Novelly RA
(1990)
Retrograde amnesia following unilateral temporal lobectomy.
Neuropsychologia
28:243-255[Web of Science][Medline].
-
Burnham WH
(1903)
Retroactive amnesia: illustrative cases and a tentative explanation.
Am J Psychol
14:382-396[Web of Science].
-
Fujii T,
Moscovitch M,
Nadel L
(2000)
Memory consolidation, retrograde amnesia and the temporal lobes.
In: Handbook of neuropsychology, Vol 2 (Cermak LS,
ed), pp 199-226. Amsterdam: Elsevier.
-
Hermann BP,
Wyler AR,
Somes G,
Duhan C,
Berry AD,
Clement L
(1994)
Declarative memory following anterior temporal lobectomy in humans.
Behav Neurosci
108:3-10[Web of Science][Medline].
-
Howell DC
(1997)
In: Statistical methods for psychology. Belmont, CA: Wadsworth.
-
Kapur N
(1999)
Syndromes of retrograde amnesia: a conceptual and empirical synthesis.
Psychol Bull
125:800-825[Web of Science][Medline].
-
Kopelman MD,
Wilson BA,
Baddeley AD
(1989)
The autobiographical memory interview: a new assessment of autobiographical and personal semantic memory in amnesic patients.
J Clin Exp Neuropsychol
11:724-744[Web of Science][Medline].
-
Kopelman MD,
Stanhope N,
Kingsley D
(1999)
Retrograde amnesia in patients with diencephalic, temporal lobe or frontal lesions.
Neuropsychologia
37:939-958[Web of Science][Medline].
-
Markowitsch HJ
(1995)
Which brain regions are critically involved in the retrieval of old episodic memories?
Brain Res Rev
21:117-127[Medline].
-
McKinnon DF,
Squire LR
(1989)
Autobiographical memory and amnesia.
Psychobiology
17:247-256.
-
Miller LA,
Munoz DG,
Finmore M
(1993)
Hippocampal sclerosis and human memory.
Arch Neurol
50:391-394[Abstract/Free Full Text].
-
Moscovitch M,
Nadel L
(1998)
Consolidation and the hippocampal complex revisited: in defense of the multiple-trace modeldiscussion point.
Curr Opin Neurobiol
8:297-300[Web of Science][Medline].
-
Moscovitch M,
Nadel L
(1999)
Multiple-trace theory and semantic dementia: response to KS Graham.
Trends Cognit Sci
3:87-89[Web of Science][Medline].
-
Nadel L,
Moscovitch M
(1997)
Memory consolidation, retrograde amnesia and the hippocampal complex.
Curr Opin Neurobiol
7:217-227[Web of Science][Medline].
-
Nadel L,
Moscovitch M
(1998)
Hippocampal contributions to cortical plasticity.
Neuropharmacology
37:431-439[Web of Science][Medline].
-
O'Connor M,
Morin M,
Verfaellie M,
Greenblatt D,
Doherty R,
Cahn G,
Schomer D
(1999)
Performance of temporal lobectomy patients on tests of remote memory.
J Int Neuropsychol Soc
5:117.
-
Reed JM,
Squire LR
(1998)
Retrograde amnesia for facts and events: findings from four new cases.
J Neurosci
18:3943-3954[Abstract/Free Full Text].
-
Rempel-Clower N,
Zola SM,
Squire LR,
Amaral DG
(1996)
Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation.
J Neurosci
16:5233-5255[Abstract/Free Full Text].
-
Ribot T
(1882)
In: Diseases of memory. New York: Appleton.
-
Sanders HI,
Warrington EK
(1971)
Memory for remote events in amnesic patients.
Brain
94:661-668[Free Full Text].
-
Scoville WB,
Milner B
(1957)
Loss of recent memory after bilateral hippocampal lesions.
J Neurol Neurosurg Psychiat
20:11-21.
-
Squire LR
(1992)
Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans.
Psychol Rev
99:195-231[Web of Science][Medline].
-
Squire LR,
Alvarez P
(1995)
Retrograde amnesia and memory consolidation: a neurobiological perspective.
Curr Opin Neurobiol
5:167-177.
Copyright © 2000 Society for Neuroscience 0270-6474/00/20155853-05$05.00/0
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|
N. Kapur and M. Prevett
Unexpected amnesia: are there lessons to be learned from cases of amnesia following unilateral temporal lobe surgery?
Brain,
December 1, 2003;
126(12):
2573 - 2585.
[Abstract]
[Full Text]
[PDF]
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E. A. Maguire and C. D. Frith
Lateral Asymmetry in the Hippocampal Response to the Remoteness of Autobiographical Memories
J. Neurosci.,
June 15, 2003;
23(12):
5302 - 5307.
[Abstract]
[Full Text]
[PDF]
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R. W.-C. Wong, M. Setou, J. Teng, Y. Takei, and N. Hirokawa
Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice
PNAS,
October 29, 2002;
99(22):
14500 - 14505.
[Abstract]
[Full Text]
[PDF]
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H. J. Spiers, N. Burgess, E. A. Maguire, S. A. Baxendale, T. Hartley, P. J. Thompson, and J. O'Keefe
Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town
Brain,
December 1, 2001;
124(12):
2476 - 2489.
[Abstract]
[Full Text]
[PDF]
|
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TOP
ABSTRACT
INTRODUCTION
