doi:10.1093/brain/awm258
Brain (2007), 130, 3184 ^3199
Autobiographical memory after temporal lobe
resection: neuropsychological and MRI
volumetric findings
M. Noulhiane,1,2 P. Piolino,3,4 D. Hasboun,1,5 S. Clemenceau,6,7,8 M. Baulac7,8 and S. Samson2,7
1
Laboratoire de Neurosciences Cognitives et d’Imagerie Ce¤re¤brale, LENA CNRS UPR 640, Universite¤ Pierre et Marie
Curie-Paris 6, CHU Pitie¤ Salpe“trie're, Paris, 2Neuropsychologie et Cognition Auditive, JE 2497, Universite¤ Charles de
Gaulle-Lille 3, Villeneuve d’Ascq, 3Laboratoire de Psychologie et Neurosciences Cognitives, CNRS FRE 2987, Universite¤ ParisDescartes, Boulogne-Billancourt, 4INSERM ^ EPHE ^ Universite¤ de Caen Basse-Normandie, Unite¤ E0218, GIP Cyceron, CHU
Co“te de Nacre, Caen, 5Service de Neuroradiologie, CHU Pitie¤ Salpe“trie're, Paris, 6Service de Neurochirurgie, CHU Pitie¤
Salpe“trie're, Paris, 7Unite¤ d’Epileptologie, CHU Pitie¤ Salpe“trie're, Paris and 8INSERM U739, Cortex et Epilepsie, Universite¤
Pierre et Marie-Paris 6, CHU Pitie¤ Salpe“trie're, Paris, France
Correspondence to: Marion Noulhiane, LPNCog CNRS FRE 2987, e¤quipe de recherche: ‘Me¤moire et Apprentissage’ 71, ave
Edouard Vaillant F-92774 Boulogne-Billancourt Cedex, France
E-mail: [email protected]
This study examined the contribution of medial temporal lobe (MTL) structures in autobiographical memory.
While some investigators have reported a temporal gradient in memory performance, characterized by
retrieval difficulties limited to recent periods of life [Squire and Alvarez (Retrograde amnesia and memory
consolidation: a neurobiological perspective. Curr Opin Neurobiol 1995; 5: 169^77)], others have suggested that
this impairment involves all life-time periods [Nadel and Moscovitch (Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 1997; 7: 217^27)]. In this study, autobiographical memory
was assessed in 22 patients who had undergone a left (n = 12) or a right (n = 10) MTL resection for the relief of
epileptic seizures and in 22 normal control participants. For this purpose, we used an autobiographical memory
task (TEMPau, Piolino et al., 2003) across four time periods covering the subjects’ entire lifespan. For each
period, an overall autobiographical memory score (AM score) was obtained, from which a strictly episodic
score (SE score), characterized by specificity and richness of details, was computed. For all events recalled,
Remember responses justified by specificity of factual, spatial and temporal contents (jR responses) were
measured using the Remember/Know paradigm. MRI volumetric analyses performed on the medial (i.e. hippocampus, temporopolar, entorhinal, perirhinal and parahippocampal cortices) and lateral temporal (i.e. superior,
middle and inferior temporal gyri) lobe structures stated that the resection mainly included MTL structures.
AM and SE scores were impaired in patients with right and left MTL resections as compared to normal controls
across all time periods, reflecting the patients’ particular difficulty in producing specific and detailed memories
across all periods. This impairment was associated with poor autonoetic consciousness, revealed by the small
number of jR responses across all periods. Results of correlation analysis between MRI volume measures
of temporal lobe structures and autobiographical memory scores suggest that the right MTL structures are
particularly responsive in reliving the encoding context regardless of remoteness. Our results support the bilateral MTL contribution to episodic autobiographical memory covering the entire lifespan, which is consistent
with the multiple trace theory of MTL function [Moscovitch et al. (Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 2005; 207: 35^66.)].
Keywords: autobiographical memory; autonoetic consciousness; temporal lobe epilepsy surgery; MRI volumetric analysis
Abbreviations: MTL = medial temporal lobe; TLE = temporal lobe epilepsy; TPC = temporopolar cortex; PRC = perirhinal
cortex; EC = entorhinal cortex; PHC = Parahippocampal cortex
Received April 17, 2007. Revised September 24, 2007. Accepted October 1, 2007. Advance Access publication November 6, 2007
ß The Author (2007). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: [email protected]
Autobiographical memory after TLE surgery
Introduction
It is generally accepted that damage to the hippocampus
and related medial temporal lobe (MTL) structures leads to
severe anterograde memory deficits. This finding has been
well documented in patients who have undergone MTL
resection for the relief of intractable epilepsy (e.g. Milner
et al., 1968; Milner, 1975; Smith and Milner, 1981; Saykin
et al., 1989; Hermann et al., 1992; Helmstaedter and Elger,
1996; Berenbaum et al., 1997). However, relatively few
studies have examined retrograde memory impairments and
in particular, episodic autobiographical memory in these
same patients. Autobiographical memory refers to a multifaceted concept encompassing different kinds of knowledge,
from general knowledge about oneself (semantic component) to very specific personal events related to the self
(episodic component) (Tulving et al., 1988; Kopelman
et al., 1989; Conway and Pleydell-Pearce, 2000). This
memory ability appears to be necessary to construct a sense
of identity and continuity. More specifically, episodic
autobiographical memory refers to personally relevant
events acquired in a specific spatio-temporal context and
characterized by an autonoetic state of consciousness
(Tulving, 1985). This latter component enables conscious
recollection of a personal event in its original encoding
context and implies a kind of mental time travel involving
a personal subjective experience of remembering. Hence,
episodic autobiographical memory contains specific
‘sensory-perceptual-cognitive-affective
details’
(Conway,
2001; Conway and Holmes, 2004) that elicit the autonoetic
experience of mentally reliving a past event. In contrast,
semantic autobiographical memory is characterized by
a noetic state of consciousness allowing one to retrieve
general facts about an event without re-experiencing it.
In neuropsychology, several investigations involving
single-case or group studies have examined autobiographical memory in epileptic patients tested before or after
temporal lobe resection. However, their results are still
controversial regarding the impact of unilateral lesions on
the extent of retrograde autobiographical memory deficit.
The differences between the methods used to assess
autobiographical memory, the severity of the epilepsy or
the extent of the resection may be responsible for such
discrepancies. In 1957, Scoville and Milner reported the
case of HM who had undergone a bilateral MTL removal
to control intractable epilepsy (Scoville and Milner, 1957).
The initial evaluation of HM’s retrograde memory, based
on post-operative interviews, indicated an autobiographical
retrograde amnesia for a period of 3 years prior to his
surgery. Further evaluations of HM’s autobiographical
retrograde memory using more detailed testing methods
revealed impairments extending 11 years back (Corkin,
1984) or even longer (Corkin, 2002). By applying a stringent new scoring method proposed by Levine et al. (2002),
Steinvorth et al. (2005) showed that HM presented retrograde amnesia for episodic components of autobiographical
Brain (2007), 130, 3184 ^3199
3185
events throughout his entire life without a temporal gradient, whereas personal semantic and generic memories were
spared. This finding emphasized the permanent involvement of MTL structures in retrograde memory. Barr et al.
(1990) further explored this issue in a group of patients
who had undergone unilateral temporal lobectomy using an
extensive battery of remote memory tests tapping into
episodic and semantic personal memories. They found that
only patients with left temporal lobectomy showed remote
autobiographical memory impairments. Using a standard
test of autobiographical memory (AMI, Kopelman et al.,
1989), Viskontas et al. (2000) found that patients with
either right or left MTL damage had a poorer memory for
autobiographical events than normals, even for those dating
from early childhood, suggesting that both left and right
temporal lobe lesions affect autobiographical memory.
These deficits, which were also present in patients with
late-onset seizures, were noted in pre- and post-surgical
cases. Conversely, personal semantic memory was not
impaired. By using an autobiographical fluency task
developed by Dritschel et al. (1992), Lah et al. (2004)
assessed retrieval of names of personal acquaintances
(i.e. personal semantic memory) or of personal events
(i.e. episodic memory) in patients who had undergone
unilateral temporal lobectomy. These authors found that
patients generated significantly fewer names than controls
but there was no group difference for personal event
fluency. More recently, Lah et al. (2006), using the same
task in patients with right and left temporal lobe epilepsy
(TLE), reported that the two patient groups were impaired
in the subtest of fluency names. In the personal event
fluency, however, they found that patients with right TLE
were more impaired than patients with left TLE.
Voltzenlogel et al. (2006) also showed that patients with
both right and left temporal lobe epilepsy produced deficits
in memory for autobiographical episodes assessed by
the AMI and the Modified Crovitz Test (Crovitz and
Schiffman, 1974; Graham and Hodges, 1997) across all time
periods. In addition, an effect of laterality was noted, with
right TLE patients obtaining significantly better scores than
left TLE patients. In contrast, personal semantic memory
was spared in both groups. Except in the study of Lah et al.
(2006) which found that young age at onset (younger than
14 years) was associated with greater difficulties in recall
of famous events, all these studies agreed that the duration
of epilepsy and the age of seizure onset did not influence
performance on remote memory measures. In brief, the
recent neuropsychological findings in epileptic patients
obtained before or after MTL resection attested to the
preservation of personal semantic memory but generally
showed deficits of episodic autobiographical memory.
The issue of the impact of unilateral lesions is still a
matter for debate.
The temporally graded or un-graded episodic retrograde
memory impairments found in epileptic patients with
temporal lobe resection can be explained by two competing
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neurobiological models of long-term episodic memory.
According to the standard model (McClelland et al., 1995;
Squire and Alvarez, 1995; Murre, 1996; Bayley et al., 2005),
MTL structures are not only involved in encoding but they
may also contribute to storage and retrieval of declarative
memory (either episodic or semantic) for a limited period
of time (i.e. few years). The MTL would serve as a temporary index for retrieval, whereas the neocortex would
provide permanent long-term memory repositories. After a
couple of years (Graham and Hodges, 1997; Schmidtke and
Vollmer, 1997) or approximately 10 years (Rempel-Clower
et al., 1996; Reed and Squire, 1998), the links between the
MTL and the neocortex vanish. This model therefore
predicts a temporally graded retrograde memory deficit
of episodic information in patients with MTL resection.
An alternative model, the multiple trace model, suggests
that the hippocampus and related MTL structures are
permanently involved in the recollection of episodic
memories (Nadel and Moscovitch, 1997, 2001; Nadel and
Hardt, 2004; Moscovitch et al., 2005). As time passes, new
links are created within the MTL so that remote episodic
memories are stored even more deeply in multiple traces,
i.e. represented by multiple hippocampal–neocortical traces.
This theory gives a comprehensive account of episodic
retrograde memory deficits observed in patients with
MTL lesions (see Fujii et al., 1999; Cipolotti et al., 2001;
Rosenbaum et al., 2001; Moscovitch et al., 2005). The MTL
is therefore necessary to re-experience detailed episodic
memories no matter how old they are. This model suggests
that the MTL may permanently contribute to the different aspects of episodic autobiographical memory but it
provides no indication about the specific involvement of
each MTL structure in such memory abilities (Moscovitch
et al., 2005). In this current debate on the role of MTL
structures in episodic autobiographical memory, anatomical
data describing the extent damage within the temporal lobe
constitute precious findings.
The aim of the present study was therefore to investigate the
role of various MTL regions in episodic autobiographical
memory in patients who had undergone unilateral MTL
resection for the relief of intractable epilepsy. For this purpose,
we used an autobiographical memory task (TEMPau task,
Piolino et al., 2003) that allows one to obtain a stringent score
of episodicity and to differentiate Remember from Know
responses (Tulving, 1985; Gardiner, 2001) by asking factual,
spatial and temporal details associated with specific personal
events. A ‘Remember’ response corresponds to the retrieval of
an event based on the recollection of details about the source
of acquisition. A ‘Know’ response corresponds to a feeling
of familiarity without any precise recollection. This task has
previously been used to specify features of episodic autobiographical memory deficits in ageing, neurodegenerative
diseases and traumatic brain injury as well as psychiatric
diseases (e.g. Piolino et al., 2003, 2004, 2006, 2007), but not yet
in patients with unilateral MTL resection. We quantified the
remaining temporal lobe tissue after the resection by means
M. Noulhiane et al.
of MRI volumetric measures of MTL structures (i.e. the
temporopolar, perirhinal, entorhinal and parahippocampal
cortices and the hippocampus). To ensure that the resection
mainly concerned the MTL structures, we also performed
MRI volumetric analysis of the lateral temporal lobe structures (i.e. the superior, middle and inferior temporal gyri).
We used a correlative approach between episodic autobiographical memory measures across different time periods
(recent and remote periods) and MRI volumetric measures
(see Kopelman et al., 2003; Gilboa et al., 2005) of medial and
lateral temporal lobe structures. According to the standard
model, we predicted correlations between remaining volumes
of the MTL and episodic memory deficits for recent but not
remote periods. Conversely, if the multiple trace model is
valid, correlations between remaining volumes of the MTL
and episodic memory deficits regardless of the time period
would be expected.
Methods
Participants
Twenty-two patients who had undergone a left (LTR, n = 12)
or right (n = 10) MTL resection for the relief of medically
intractable epilepsy associated with hippocampal sclerosis (diagnosed by pre-operative MRI) and 22 normal controls participated
in this study. The patients were operated at La Salpêtrière Hospital
(Paris). Patients underwent a temporal lobe resection by using the
transcortical approach across the superior temporal gyrus (Fig. 1).
The resections, performed microsurgically under operative microscope by the same neurosurgeon (SC), included the removal of the
major portion of the amygdala (with respect of its most medial
and superior parts), the uncus, the hippocampus, various amounts
of the surrounding cortices (entorhinal, perirhinal and parahippocampal cortex) and the anterior portion of the superior
temporal gyri caudally to the temporal pole. The temporal pole
was resected in all patients except for two RTR patients and
one LTR patient for whom the surgery consisted of a selective
amygdalo-hippocampectomy. Besides the temporal pole, the
lateral and basal temporal lobe cortices, except the most anterior
part of the superior temporal gyrus, were preserved in all patients.
The patients underwent imaging with a 1.5-T MRI scanner
using a standard head coil and tilted coronal 3D magnetizationprepared rapid acquisition gradient-echo sequence with the
following parameters: 14.3/6.3/1 (repetition time/echo time/
excitation). This resulted in 124 contiguous T1-weighted partitions with a 1.5-mm section thickness. High-resolution MRI
volumetric measurements of the gray-matter of MTL structures
including the temporopolar cortex (TPC), perirhinal cortex
(PRC), entorhinal cortex (EC), parahippocampal cortex (PHC)
and hippocampus (H), were carried out using a protocol
developed by Noulhiane et al. (2006). We also measured gray
matter volumes of the lateral temporal lobe structures, namely the
superior temporal gyrus (STG), the middle temporal gyrus (MTG)
and the inferior temporal gyrus (ITG) in reference to the protocol
of Onitsuka et al. (2004). T1-weighted images were used in an
automatic segmentation program to classify brain tissue into gray
and white matter (Brainvisa environment, Cointepas et al., 2001).
In this protocol, the most anterior part of the STG, MTG and
ITG, as it could be considered as the temporal pole (Broadmann’s
area 38), was not included. We added the measure of the STG,
Autobiographical memory after TLE surgery
Brain (2007), 130, 3184 ^3199
3187
Table 1 Mean of gray matter volumes (S.D.) in cm3 of right
and left medial (hippocampus, temporopolar, perirhinal,
entorhinal and parahippocampal cortices) and lateral
temporal lobe structures in patients with right (RTR)
and left (LTR) temporal lobe resection
Cortices
Fig. 1 Illustration of a right anteromedian temporal lobe resection
in 3D rendering from latero-frontal (top) and medio-frontal
(bottom) view. As showed, the resection was centred on the
MTL structures.
MTG and ITG, which extended along the temporal pole in
accordance with their anatomical definition (Duvernoy, 1988)
and to the boundary of the temporopolar cortex (Insausti et al.,
1998; Noulhiane et al., 2006). The most anterior coronal slice in
which the temporal stem could be seen was considered as the
boundary between the region corresponding to the temporal
pole (i.e. anterior) and those obtained in the caudal section
(i.e. posterior). Overall, our measures encompassed the rostrocaudal extent of each temporal lobe structures and allowed us
to distinguish the volumes of medial and lateral temporal lobe
structures. As shown in Table 1, the volumes of MTL structures
from the hemisphere ipsilateral to the surgery were significantly
reduced compared to the contralateral one (Ps50.01, Wilcoxon
comparisons) as well as the volumes of the most anterior portion
of lateral temporal lobe structures which included in the temporal
pole (Ps50.05, Wilcoxon comparisons). In contrast, there were no
differences between the volumes of posterior lateral temporal lobe
structures of both hemispheres (Ps40.05, Wilcoxon comparisons).
The remaining volumes of all temporal lobe structures did not
differ between patients with right or left temporal lobe resection
(Ps40.05; Mann–Whitney comparisons) indicating that there
was no difference in the extent of the removal between the two
patient groups.
Right hemisphere
Temporopolar
RTR group
0.56 0.38
LTR group
3.11 0.28
Perirhinal
RTR group
0.61 0.24
LTR group
2.56 0.21
Entorhinal
RTR group
0.40 0.15
LTR group
1.57 0.69
Parahippocampal
RTR group
1.64 0.16
LTR group
2.16 0.10
Hippocampus
RTR group
0.22 0.07
LTR group
4.06 0.26
Superior Temporal Gyrus
Anterior
RTR group
0.23 0.31
LTR group
1.18 0.38
Posterior
RTR group
8.61 0.89
LTR group
9.16 1.58
Middle Temporal Gyrus
Anterior
RTR group
0.10 0.19
LTR group
1.12 0.17
Posterior
RTR group
8.99 1.10
LTR group
10.41 1.25
Inferior Temporal Gyrus
Anterior
RTR group
0.06 0.15
LTR group
0.56 0.50
Posterior
RTR group
8.17 1.19
LTR group
8.93 1.00
Left hemisphere
2.91 0.18
0.10 0.34
2.16 0.20
0.50 0.14
1.49 0.57
0.36 0.07
2.26 0.17
1.47 0.13
3.36 0.27
0.32 0.05
1.34 0.25
0.55 0.48
9.11 1.90
8.48 0.96
1.20 0.44
0.22 0.67
9.64 1.74
9.86 1.43
0.44 0.27
0.04 0.12
8.44 1.35
9.41 1.10
As noted in Table 2, febrile seizures were reported in 21 out of
the 22 patients and the age of seizure onset did not differ between
the two patient groups (Z = 1.45; P = 0.14; Mann–Whitney
comparisons). Patients with bilateral electroencephalographic
abnormality, evidence of fast-growing tumours and diffuse
cerebral damage as well as those with a Full-Scale IQ (Wechsler
Adult Intelligence Scale-Revised) under 75 or atypical speech
representation, as determined by intracarotid sodium Amytal
testing (Wada and Rasmussen, 1960) or by fMRI, were excluded
from this study. Patients were tested between 6 months and
8 years post-operatively but the majority were tested at 6 months
(RTR = 7; LTR = 7). According to Engel’s classification (Engel
et al., 1993), 20 patients were seizure-free (class I) and two
patients presented rare seizures (class II) at the time of testing.
All patients were still taking medication excepted for two patients
in each group who stopped medication. The normal controls
(NC) had no neurological or psychiatric history and no medication known to impair memory was allowed. They were selected
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M. Noulhiane et al.
Table 2 Demographic information for patients with right (RTR) and left (LTR) temporal lobe resection
and normal controls (NC)
Sex
Age (years)
Education (years)
Aetiology, age
Antiepiletic drug
Seizure onset, age
Post-operative period
RTR
LTR
NC
6M/4F
34.3 9.9
13.1 3.5
10 FC (12 months 6.1)
8 on/2 off
15.2 7.8 (years)
2.1 2.8 (years)
6M/6F
34.2 7.5
12 2.5
11 FC (8.8 months 4.6)/1 patient at 11 years
10 on/2 off
11.6 8.3 (years)
1.7 1.5 (years)
12M/10F
34 8.5
12.4 2.7
^
^
^
^
FC = Febrile convulsion.
Table 3 Neuropsychological test scores for patients with right (RTR) and left (LTR) temporal lobe resection
and normal controls (NC)
Neuropsychological Tests
RTR
LTR
NC
WAIS-R (Full-Scale IQ)
Auditory-verbal span
Forward
Backward
Visuo-spatial span Forward
RAVLT (max. 15)
First recall
Fifth recall
Delayed recall
Information (WAIS-R)
Similarities (WAIS-R)
DO 80 (max. 80)
94.7 12.4
92.9 8.9
^
Scaled scores
7.2 1.5
5.4 2.1
5.8 1.1
6.7 1.5
4.7 1.2
6 1.1
^
^
^
Raw scores
Raw scores
Raw scores
6.9 1.2
12.6 1.8
10.2 2.9
8.4 3.0
9.2 1.8
79.5 0.9
6.3 2.3
10.6 2.4
8.4 4.2
7.5 3.0
8.3 2.1
77.3 2.0
8.3 2.2
14.3 0.8
13.7 1.2
10 3
10 3
79.3 1
Type of scores
Raw scores
Raw scores
Raw scores
Scaled scores
Scaled scores
Raw scores
DO80 = Oral test of denomination [in French: Test de de¤nomination orale d’images]; RAVLT = Rey Auditory Verbal Learning test;
WAIS-R = Wechsler Adult Intelligence Scale-Revised.
to match the patients as closely as possible in terms of age, sex
and education (Table 3). All participants were right-handed and
gave their informed consent in writing before testing in
accordance with the Declaration of Helsinki.
Table 3 displays additional neuropsychological data: mean
Full-Scale IQ (WAIS-R), auditory-verbal (digit) and visuo-spatial
(block) spans, along with results of the first, fifth and delayed
(30 min) recall trials and recognition of words from the Rey
Auditory Verbal Learning test (RAVLT, Rey, 1964) as well as
semantic memory performance assessed with two WAIS-R subtests
‘information’ and ‘similarities’ and a test of denomination
(DO 80, Deloche and Hannequin, 1997). Non-parametric analyses
were performed: Mann–Whitney U tests to compare each group’s
performance and Kruskal–Wallis analyses of variance (ANOVAs)
by ranks to compare all three groups (RTR, LTR and NC).
The results revealed no differences between the two patient groups
in terms of Full-Scale IQ (Z = 0.16; P = 0.87). There were also no
differences between the two patient groups in terms of auditoryverbal span (Z = 0.53; P = 0.59), forward span (Z = 0.15; P = 0.88)
and visuo-spatial span (Z = 0.82; P = 0.41). In the RAVLT, the
analysis carried out on the sum of free recalls revealed a significant
effect of Group [H(2,41) = 15.85; P50.001], with the LTR patients
recalling fewer words than the RTR (P50.05) and NC (P50.05)
groups. The results of the delayed recall task revealed a significant effect of Group [H(2,41) = 16.29; P50.001], with the LTR
(P50.001) and RTR groups (P50.05) recalling fewer words than
the NC group. The results revealed that semantic memory
performance was within the range of the normative data for
the two patient groups as indicated by the scores obtained in the
WAIS-R subtests ‘information’ and ‘similarities’ and in the
denomination test. No significant differences were found between
the two patient groups excepted for the denomination task, with
LTR patients producing fewer errors than RTR ones (P50.01).
However, no patients obtained a score below the cut-off.
Material
Autobiographical memory assessment
To assess autobiographical memory, we used a shortened version of a semi-structured questionnaire (TEMPau
task, Piolino et al., 2003; for more complete details see
Piolino et al., 2006, 2007) based on previously published
paradigms (Borrini et al., 1989; Kopelman et al., 1989;
Piolino et al., 2002).
Procedure
This test investigated the ability to recall in detail specific
events situated in time and space from four time periods
Autobiographical memory after TLE surgery
[P1: 0–17 years old, P2: 18–30 years old, P3: the last 5 years
(except the last 12 months) and P4: the last 12 months]
as well as the subjective states of conscious awareness
associated with such memories (Tulving, 1985, 2002). Since
the average age of the participants was 34 years, this procedure covered their whole life. Very precise instructions,
emphasizing the notions of specificity (i.e. unique event
lasting less than a day, with spatial and temporal location)
and the reliving of affective-sensory-perceptual details were
given to the participants.
The ability to recall memories from each time period,
except the last one (the most recent lifetime period), was
assessed using four topics (a meeting or an event linked to
a person, a school or professional event, a trip or journey,
a family event). For the most recent lifetime period, eight
questions were asked in order to conduct a chronological
study of the recent past (last summer, last Christmas or
last New Year’s Eve, last month, last weekend, 2 days ago,
yesterday, today).
Immediately after each recall, the participants were asked
to indicate the subjective states of conscious awareness
associated separately with the recall of what happened (the
factual content), where (the place) and when (the time),
always in this order. They were instructed to give
a Remember, Know or Guess response (Mantyla, 1993)
according to whether each aspect of the recalled event was
associated with conscious recollection, simply knowing
or guessing, respectively. A Remember response was defined
as the ability to mentally relive specific aspects such as
perceptions, thoughts or feelings that occurred or were
experienced at the time of the event. The participants were
asked to give details aloud to ensure that they were using
Remember responses properly. An example of a consistently
recollected memory refers to a meeting (the participant
recollected very specific details of the scene, his/her feelings
and thoughts) that took place in a particular environment
(the participant relived the specific atmosphere, his/her
position in the scene) 2 years ago (the participant recollected the thoughts he had with regard to the fact that the
meeting took place exactly 5 years after his school graduation, the time of day). A Know response was described
as simply knowing what happened, where and when, but
without this knowledge being accompanied by any
conscious recollection (in an example like the one above,
the participant simply knew he/she had attended this
meeting). A Guess response corresponded to aspects of the
event that were neither consciously recollected nor simply
known, but guessed (the participant guessed the meeting
he/she attended took place 2 years ago).
Scoring
Each event was scored on a 5-point scale as proposed by
Baddeley and Wilson (1986). This scale took into account
the specificity of the content (single or repeated event),
its spatio-temporal situation and the presence of details
Brain (2007), 130, 3184 ^3199
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(perceptions, thoughts, feelings). A specific event without
any details but situated in time and space scored 3 points.
A repeated or extended event scored 2 points or 1 point
according to whether or not it was situated in time and
space. The absence of any recollection, or only general
information about the topic, was scored 0. Two different
total scores were calculated for each period: (i) an overall
autobiographical score (AM), which included all scores
regardless of their nature (max. 4 4 = 16), and corresponded to the classic episodic memory score used in the
well-known AMI (Kopelman et al., 1989); (ii) a strictly
episodic score (SE), which used a stringent criterion,
including only the most episodic memories, i.e. memories
scoring 4 (max. 4 4 = 16).
For the purpose of this study, we focussed our interest
on the proportion of Remember (R) responses rather than
Know and Guess responses. We also used a procedure
to check the R responses for specificity. In this way,
we considered R responses as justified when they corresponded to specific memories scoring 4 or 3. Thus, justified
R (jR) was expressed as a percentage per period (number
of the justified R responses divided by the number of
memories recalled100) for each content (what, where,
when) or globally with the overall content. For example, the
‘where jR’ score corresponded to the ratio of R responses
per period given for the spatial features of the recalled
events when they corresponded to a memory scored 4 or 3.
The mean jR responses obtained for ‘what’, ‘where’ and
‘when’ was used to compute the percentage of total jR
responses (% total jR responses) per period. For each score,
we recorded the results for the period corresponding to
the last 12 months, which had eight items instead of four.
We conducted a retest 15 2 days after the initial task
to check each memory by using a cued recall task which
involved asking the subjects to recall in random order the
content and spatio-temporal situation of each memory.
Two independent experts (MN and PP) rated each memory
until a consensus was reached.
Data analysis
Autobiographical memory retrieval tasks
Because of the small patient groups and the variability
of the data, non-parametric statistics were used throughout
the analysis of the autobiographical memory test, expressed
in terms of a total score per period. Kruskal–Wallis analyses
were carried out to examine the influence of group (RTR,
LTR and NC) as a between-subject factor on memory
scores and Mann–Whitney U tests were then conducted
to determine group differences across each time period.
To test the effect of period within each group, Friedman
analyses were performed. For Remember responses, these
analyses included the content (what, where, when) as
within-subject factor. Wilcoxon tests were then processed
individually for each group to determine differences
3190
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M. Noulhiane et al.
between each period (P1: 0–17 years old; P2: 18–30 years
old; P3: last 5 years; P4: last 12 months).
Relationships between autobiographical memory scores
and volumetry of temporal lobe structures
Spearman’s rank–order correlations were performed
between volumetric measurements, taking into account
the lateralization of the resection, and autobiographical
memory scores. The latter corresponded to the AM, SE
and total jR scores for the recent (combining P3 and P4)
and the remote (combining P1 and P2) periods. To better
delineate what best characterized episodicity, we conducted
stepwise regression analyses to predict the autobiographical
memory measures, either for the recent past or the remote
past, using the volumetric values as predictors. Stepwise
regression analyses are a special case of forward selection
of predictive independent variables: in addition to the steps
performed in the forward selection algorithm, all variables
were tested if their contribution was significant after a
new variable had been added. This led to the elimination
of an already selected variable, if this variable had become
superfluous because of its relationship to the other
variables. The stepwise method employs a combination of
the procedures used in the forward entry and backward
removal methods. Then, we carried out a multiple regression on the significant predictive variables selected by the
stepwise regression, including tables to show the regression
coefficient and associated significance probability of each
variable. Considering the small number of patients per
group, these regression analyses were exploratory. A statistical threshold of P50.05 was considered as significant.
Analyses of epilepsy variables
Relationships between every autobiographical memory
measure for each period and epilepsy variables (age of
seizure onset and post-operative delay) were calculated
using Spearman’s rank–order correlation in both patient
groups considering the lateralization of the resection.
Results
Unlike control subjects, who responded to all autobiographical questions, the RTR group responded to 91% and
the LTR to 90.4% of the questions (Fisher’s exact test,
P50.001), but no significant difference was found between
the two patient groups. In all three groups of participants,
all the memories that were given at the test were also given
at the retest.
Autobiographical memory retrieval tasks
Overall autobiographical memory score
Figure 2 displays the results of statistical analyses for the
AM score for the three groups of participants as a function
of time period. The group comparisons for each time
period revealed significant differences. The two patient
Fig. 2 Autobiographical memory score (AM) according to time
period in patients with left (LTR, n = 12) or right (RTR, n = 10)
MTL resection and normal control participants (NC, n = 22).
Planned comparisons to illustrate the Group effect for each
period as indicated in the figure. P = Period, P1 = 0 ^17 years old,
P2 = 18 ^30 years old, P3 = last 5 years; P4 = last 12 months,
P_0.05; P_0.01, P_0.001. (Bars indicate the standard
errors of the mean.)
groups were impaired across all periods in comparison to
the NC group (from Ps50.001 to Ps50.05). Moreover,
no significant difference was found between the RTR and
LTR groups. Otherwise, the comparisons of the performance at different time periods showed a ‘recency effect’ in
the NC group (P44P1, P50.01; P44P2, P50.05; P44P3,
P50.01) but not in the RTR and LTR groups. However,
a tendency (P = 0.07) was observed in the LTR group, with
performance for P2 being better than for P3 and P4 (for
details, see Table 4 and Fig. 2 for planned comparisons).
Strictly episodic autobiographical memory score
Figure 3 displays the results for the strictly episodic
autobiographical memory score (SE) for the three groups
of participants as a function of time period. The group
comparisons for each time period revealed that both patient
groups were impaired in comparison to the NC group
across all time periods. No significant differences were
found between the two patient groups although a tendency
was observed in P2, where the LTR group performed better
than the RTR group (P = 0.06). Otherwise, comparisons of
performance for different time periods within each group
showed that performance tend to decrease with remoteness
in the NC (P = 0.07), but not in the LTR or RTR groups
(for details, see Table 4)
To sum up, the results showed impairments in both
the RTR and the LTR groups in the AM or SE scores.
The data emphasized that patients found it difficult to
retrieve single events, located in time and in space, with
phenomenological details (perceptions, thoughts, feelings)
related the source of acquisition. The LTR group,
however, had a tendency to report more memories for
the 18–30 period (the so-called autobiographical memory
Autobiographical memory after TLE surgery
Brain (2007), 130, 3184 ^3199
3191
Table 4 Summary of statistical results of autobiographical
memory scores for patients with right (RTR) and left
(LTR) temporal lobe resection and normal controls (NC):
Overall Autobiographical Memory [AM] and Strictly
Episodic [SE] scores
Autobiographical memory scores
Results
Overall Autobiographical Memory [AM] score
Between subjects
P1
H(2,44) = 9.94
P2
H(2,44) = 12.23
P3
H(2,44) = 14.45
P4
H(2,44) = 31.13
Within subjects
LTR
2(12,3) = 6.93 (P = 0.07)
RTR
2(10,3) = 1.13
NC
2(22,3) = 8.56
Strictly Episodic [SE] score
Between subjects
P1
H(2,44) = 11.46
P2
H(2,44) = 19.25
P3
H(2,44) = 17.20
P4
H(2,44) = 29.90
Within subjects
LTR
2(12,3) = 3.66
RTR
2(10,3) = 2.10
NC
2(22,3) = 6.87 (P = 0.07)
P = Period; P1 = 0 ^17 years old; P2 = 18 ^30 years old; P3 = last
5 years; P4 = last 12 months.
P50.05; P50.01, P50.001.
Fig. 4 Percentage of total justified Remember responses according to time period in patients with left (LTR, n = 12) or right
(RTR, n = 10) MTL resection and normal control participants
(NC, n = 22). Planned comparisons to illustrate the Group effect
for each period as indicated in the figure. P = Period, P1 = 0 ^17
years old, P2 = 18 ^30 years old, P3 = last 5 years; P4 = last
12 months, P_0.05; P_0.01, P_0.001. (Bars indicate the
standard errors of the mean.)
Ribot’s (1881) temporal gradient of deficits in both patient
groups (i.e. greater impairment in the recall of the recent as
compared to previous periods). Nevertheless, both patient
groups were clearly deficient regardless of the time periods.
Remember responses: autonoetic consciousness
Fig. 3 Strictly episodic memory score (SE) according to time
period in patients with left (LTR, n = 12) or right (RTR, n = 10)
MTL resection and normal control participants (NC, n = 22).
Planned comparisons to illustrate the Group effect for each
period as indicated in the figure. P = Period, P1 = 0 ^17 years old,
P2 = 18 ^30 years old, P3 = last 5 years; P4 = last 12 months,
P_0.05; P_0.01, P_0.001. (Bars indicate the standard
errors of the mean.)
‘reminiscence bump’) than the RTR group. Given that the
controls showed a recency effect in their performance
(i.e. better scores in the recall of the recent as compared
to previous periods), our results might suggest a ‘relative’
Figure 4 displays the percentage of total Remember
responses (justified in terms of specificity;% total jR
responses) according to Group and Period. The group
comparisons for each time period revealed that both patient
groups were impaired in comparison to the NC group
across all periods. Nevertheless, the deficits of patients
tended to increase with remoteness. No significant differences were found between the two patient groups.
Otherwise, the comparisons of performance at different
periods within each group showed that performance
decreased gradually with remoteness in the NC group
(P44P1, P50.001; P44P3, P50.05; P44P2, P50.05,
P34P1, P50.05; P24P1, P50.05). Although this effect
occurred in the two patient groups, it did not reach
statistical significance (for details, see Table 5).
Figure 5 shows the results of the state of consciousness
assessment (% jR responses) according to group, period
and type of information (what, where and when).
For ‘what’, the group comparisons for each time period
showed that both patient groups were impaired in comparison to the NC for all periods. No significant differences
were found between the two patient groups except for P2,
in which the RTR group performed significantly worse
than the LTR group. For ‘where’, the results showed that
the LTR group was impaired compared to the NC group
for the recent (P3 and P4) but not the remote periods
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Brain (2007), 130, 3184 ^3199
M. Noulhiane et al.
Table 5 Summary of statistical results of autonoetic
consciousness for patients with right (RTR) and left (LTR)
temporal lobe resection and normal controls (NC):
justified Remember [jR] score
Autobiographical memory scores
% total jR
Between subjects
P1
P2
P3
P4
Within subjects
LTR
RTR
NC
% what jR
Between subjects
P1
P2
P3
P4
Within subjects
LTR
RTR
NC
% where jR
Between subjects
P1
P2
P3
P4
Within subjects
LTR
RTR
NC
% when jR
Between subjects
P1
P2
P3
P4
Within subjects
LTR
RTR
NC
Results
H(2,44) = 15.02
H(2,44) = 20.60
H(2,44) = 11.51
H(2,44) = 15.47
2(12,3) = 6.33
2(10,3) = 6.97
2(22,3) = 18.83
H(2,44) = 14.51
H(2,44) = 15.87
H(2,44) = 12.49
H(2,44) = 19.42
2(12,3) = 8.34
2(10,3) = 3.55
2(22,3) = 8.15
H(2,44) = 7.01
H(2,44) = 9.84
H(2,44) = 8.89
H(2,44) = 8.46
2(12,3) = 3.16
2(10,3) = 0.94
2(22,3) = 1.56
H(2,44) = 13.15
H(2,44) = 18.74
H(2,44) = 1.31
H(2,44) = 8.51
2(12,3) = 15.44
2(10,3) = 12.54
2(22,3) = 19.76
P = Period; P1 = 0 ^17 years old; P2 = 18 ^30 years old; P3 = last
5 years; P4 = last 12 months.
P_0.05; P_0.01, P_0.001.
(P1 and P2); conversely, the RTR group was impaired
for the remote (P1 and P2) but not for the recent periods
(P3 and P4). No significant difference was found between
the two patient groups. For ‘when’, the results revealed that
both patient groups were impaired compared to the NC
group in the remote period (P1 and P2) and the LTR group
was also impaired in P4. The comparisons of performance
at different time periods within each group were carried out
regarding the type of information. Overall, the results
revealed that performance decreased with remoteness in the
NC group for ‘what’ (P44P1, P50.05; P34P1, P50.05)
and ‘when’ (P44P3, P50.01; P44P2, P50.05; P44P1,
Fig. 5 Percentage of justified Remember responses for (A) ‘what’,
(B) ‘where’, (C) ‘when’ according to time period in patients with
left (LTR, n = 12) or right (RTR, n = 10) MTL resection and normal
control participants (NC, n = 22). Planned comparisons to
illustrate the Group effect for each period as indicated in the
figure. P = Period; P1 = 0 ^17 years old, P2 = 18 ^30 years old,
P3 = last 5 years; P4 = last 12 months, P50.05; P50.01,
P50.001. (Bars indicate the standard errors of the mean.)
Autobiographical memory after TLE surgery
P50.001; P24P1, P50.01) but not for ‘where’. This effect
was significant in the LTR group for ‘what’ (P24P1,
P50.05; P24P4, P50.05) and ‘when’ (P44P1, P50.01;
P44P2, P50.05; P34P1, P50.05; P24P1, P50.05) and
in the RTR group only for ‘when’ (P44P3, P50.01;
P44P2, P50.01; P44P1, P50.01; P34P2, P50.05;
P34P1, P50.05) (Table 5).
Relationships between autobiographical
memory scores and volumetry of
temporal lobe structures
Correlation analysis
No significant correlation was found between the anterior
and posterior lateral temporal lobe structures and the AM,
the SE and the total jR scores neither for the remote nor for
the recent periods. The results revealed significant correlations between the AM score for remote periods and the
right PHC ( = 0.95; P50.001). The SE score for recent
periods correlated with the left PRC ( = 0.64; P50.05).
We also found significant correlations between the total jR
score for remote periods and the right PHC ( = 0.73;
P50.05), whereas the total jR score for recent periods
correlated with the left hippocampus ( = 0.91; P50.05).
Regression analysis
Since no correlation was obtained between the memory
scores and the volumes of lateral temporal lobe structures,
the following analyses focussed on the MTL structures.
The results of the stepwise regression analysis are displayed
in Table 6. Considering the small number of patients
per group, these results should be considered with caution.
Overall, this second exploratory analysis refined the
previous data. The results suggest that autobiographical
memory scores for remote periods were predominantly
predicted by right MTL structures while those of recent
periods appeared more dependent on bilateral MTL
structures.
Epilepsy variables
There was no correlation between age of seizure onset or
post-operative delay and any autobiographical memory
measures for any period. Some studies reported that antiepileptic medication has a significant impact on cognitive
skills, including remote memory (i.e. McGuire et al., 1992;
Thompson et al., 2000; Lah et al., 2004, 2006). Inspection
of the data revealed that the four patients who had ceased
medication did not behave differently from the remaining
ones that were still on medication.
Discussion
The aim of this study was to assess episodic autobiographical memory in patients who had undergone a left
or right MTL resection for the relief of epileptic seizures.
Brain (2007), 130, 3184 ^3199
3193
Table 6 Summary of regression analyses in predictive
model for autobiographical memory scores using the left
and right hippocampal (Hippocampus), temporopolar
(TPC), perirhinal (PRC), entorhinal (EC), and parahippocampal (PHC) residual volumes as independent variables
which were entered into and kept significant in the final
model of the forward stepwise regressions.a
Autobiographical
memory scores
Predictor
Cumulative P
explained
variance
R2 (%)
Overall Autobiographical Memory[AM] score
Remote period
Left volumes
^
^
Right volumes
R-PHC
91
[F(1,6) = 69.11]
Recent period
Left volumes
L-EC
28
[F(1,9) = 3.5]
Right volumes
R-PRC
53
[F(1,6) = 8.82]
Strictly Episodic [SE] score
Remote period
Left volumes
^
^
Right volumes
^b
^
Recent period
Left volumes
^
^
R-PRC
41
Right volumes
[F(1,6) = 4.31]
Total justifiedRemember[ jR] score
Remote period
Left volumes
^
^
Right volumes
R-PHC + TPC
85
[F(2,5) = 14.68; p50.01]
Recent period
Left volumes
L- Hippocampus 49
[F(1,9) = 8.81]
Right volumes
R-PRC
44
[F(1, 6) = 9.92]
^
0.001
0.09
0.02
^
^
^
0.05
^
0.03
0.01
0.06
a
Only significant predictors are included. The regression analysis
were first carried out step by step (forward stepwise regression),
resulting in potential significant predictors. The regression analysis
was then rerun including the significant variables. For each
memory score listed, results show the overall significant association of the set of medial temporal structures (hippocampus,
temporopolar, perirhinal, entorhinal and parahippocampal
cortices) and memory performance.
b
The results of the first regression analysis indicated that right
hippocampus (P = 0.02) and right PRC (P = 0.03) were significant
predictors of the SE score for remote periods. When the analysis
was run again with the right hippocampus and the right PRC
volumes as the independent variables, no significant predictors
were found.
For this purpose, we used an autobiographical memory task
(TEMPau, Piolino et al., 2003) that explores memories
across several periods covering the entire lifespan. This task
allows one to differentiate various scores that take qualitatively different information into account. In addition to
the classical AM score reported in most studies, we used
stringent measures of episodic autobiographical memory
3194
Brain (2007), 130, 3184 ^3199
by taking into account the number of specific and detailed
memories associated with phenomenological details and
autonoetic consciousness (Tulving, 1985, 2002). To the best
of our knowledge, this is the first study to assess the
specificity of details combined with autonoetic consciousness in patients who had undergone a unilateral MTL
resection for the relief of epileptic seizures. In addition, an
original feature of this study was the use of a correlative
approach between autobiographical memory measures
across remote and recent periods and MRI volumetric
measures of medial (i.e. the temporopolar, perirhinal,
entorhinal and parahippocampal cortices and the hippocampus) and lateral (i.e. the superior, middle, inferior gyri)
temporal lobe structures. This approach allowed us to
ensure that the resection mainly included the MTL
structures as well as the temporal pole, and to clarify the
involvement of these structures in episodic autobiographical
memory.
Overall autobiographical memory score
Our study revealed that patients who had undergone a
left or right MTL resection displayed difficulties in retrieving autobiographical memories across all time periods.
The contribution of bilateral MTL structures to autobiographical memory confirmed findings previously obtained
by Viskontas et al. (2000) and Voltzenlogel et al. (2006)
with another autobiographical memory task (Autobiographical Memory Interview-AMI, Kopelman et al., 1989).
This result is not surprising since the AM score measured
by the TEMPau is very similar to the episodic autobiographical score assessed by the AMI. All these studies
revealed that patients with either right or left MTL lesions
exhibited profound episodic autobiographical memory
deficits extending to the most remote periods of early
childhood. Unlike our study, Voltzenlogel et al. (2006) also
showed that patients with left MTL lesions performed
worse than patients with right MTL lesions on the AMI or
the modified version of the Crovitz Test (Graham and
Hodges, 1997), regardless of the remoteness of the period.
As proposed by the authors, this episodic autobiographical
memory deficit characterizing patients with left temporal
lobe epilepsy can be attributed, at least in part, to additional anterograde memory dysfunction affecting encoding
ability, but this interpretation needs further investigation.
Neither our results nor those of Viskontas et al. replicate
the findings obtained in Barr et al.’s (1990) study of postoperative patients, which used an extensive survey assessing
autobiographical memory without a stringent criterion
for episodicity. In this latter study, only patients who had
undergone left temporal lobe resection were found to be
impaired in both episodic and semantic autobiographical
memory. The authors examined only a small number of
patients (six in each group), and thus it seems plausible
that they were not able to demonstrate a deficit after a right
temporal lobe lesion.
M. Noulhiane et al.
Overall, the results of these studies emphasize the
bilateral contribution of the MTL in retrieving autobiographical memories across all time periods. However, our
investigation also provides new information by differentiating the overall autobiographical memory score (i.e. AM
score, as previously discussed) from the strictly episodic
score (SE score) and by assessing autonoetic consciousness.
Strictly episodic score and autonoetic
consciousness
Using a strict assessment criterion (i.e. SE score characterized by specificity and richness of details), our data
highlighted the fact that the patients were severely impaired,
as compared to the normal controls, in recalling memories
from across the entire lifespan. They presented a flat
temporal distribution of their performance compared to the
normal controls who presented the classic ‘recency effect’
(i.e. superiority in specific and detailed recent memories)
that has already been described in the literature on young
adults (Rubin and Schulkind, 1997; Piolino et al., 2002,
2006, 2007). Given this recency effect in controls, both
patient groups appear to be more specifically impaired
for the most recent time period. It is worth noting that
the SE score was clearly lower than the overall autobiographical memory score in both patient groups, reflecting
the patients’ particular difficulty in producing specific and
detailed memories across all periods. According to the
normal performance observed in semantic memory, this
difference between the two scores makes it clear that both
patient groups retrieved generic memories (i.e. semanticized
ones) more easily than strictly episodic memories. This is
in keeping with the view that personal semantic memory is
relatively spared after unilateral temporal lobe resection
(Viskontas et al., 2000). Our data therefore emphasize the
importance of considering the presence of details associated
with specific memories in order to reliably identify residual
episodic memories (Moscovitch and Nadel, 1999; Piolino
et al., 2003). Moreover, our methodology also documented
the autonoetic consciousness associated with each memory
by using a Remember/Know paradigm (Tulving, 1985;
Gardiner, 1988; Mantyla, 1993; Gardiner, 2001; Tulving,
2002). In this study, we showed that the percentage of
Remember responses justified by specificity was significantly
lower in RTR and LTR patients than in normal controls
across all time periods, suggesting that the MTL contributes
bilaterally to autonoetic consciousness. Interestingly, our
results are consistent with neuroimaging data showing
more bilateral MTL activation in healthy subjects during
conscious re-experiencing (remembering) than during
feelings of familiarity (knowing) (Eldridge et al., 2000;
Wheeler and Buckner, 2004). In the normal control participants, autonoetic consciousness decreased as a function
of the remoteness of events, confirming previous findings
(Piolino et al., 2006, 2007). However, this effect was not
observed in patient groups. Our results emphasize that
Autobiographical memory after TLE surgery
patients with unilateral MTL lesions have a deficit in
re-experiencing or reliving the past and mentally travelling
back in subjective time. More specifically, the TEMPau task,
which allows one to investigate the consistency of conscious
recollection by considering the sense of remembering
separately for factual, spatial and temporal information
(what, where and when, respectively), provides qualitative
information about the autonoetic features of autobiographical memories in those patients. Globally, the normal
control participants’ results showed that these three types of
information are retrieved to a similar extent except for the
‘when’ responses, which were less accessible for remote than
for recent periods, in keeping with previous results obtained
in young adults (Piolino et al., 2006, 2007). The data from
the two patient groups demonstrated less consistent
conscious recollection, regardless of the type of information. Our results point to the bilateral involvement of the
MTL in re-experiencing either phenomenological or spatiotemporal features of single autobiographical events, even
more with remoteness. Accordingly, some neuroimaging
studies have detected bilateral MTL activation when
subjects are engaged in the retrieval of specific autobiographical memories that are highly rated in terms of
specificity, mental imagery, richness of details, emotionality,
re-experiencing or personal significance (Ryan et al., 2001;
Piefke et al., 2003; Piolino et al., 2004; Greenberg et al.,
2005; Steinvorth et al., 2006; Viard et al., 2007). The results
for ‘what’ responses revealed that the justified sense
of reliving perceptive and affective details of events was
impaired in both patient groups, except for the 18–30-year
period in the LTR patients. Interestingly, this may reflect
the reminiscence ‘memory bump’ generally reported in
elderly subjects. The memory bump corresponds to the
superior recollection of vivid events that occurred between
the ages of 18 and 30 years as compared to recent or more
remote epochs of our life (Rubin and Schulkind, 1997;
Berntsen and Rubin, 2002). Indeed, the visual imagery,
emotion and spatial details are particularly vivid for remote
memories corresponding to this encoding period (Rubin
and Wetzler, 1986; Conway and Rubin, 1993; Fitzgerald,
1996; Rubin and Schulkind, 1997; Piolino et al., 2002,
2006). Since visual imagery, spatial details and emotional
processing in autobiographical memory have been predominantly associated with right-hemisphere function
including the temporal lobe structures (Fink et al., 1996;
Conway, 2001; Piolino et al., 2004), we can suggest that
patients with left temporal lobe lesions but relatively spared
right temporal lobe structures were able to use these cues
to retrieve specific phenomenologically detailed events.
For ‘where’ responses, the results revealed that the RTR
group was impaired in recalling the most remote periods
(P1 and P2), whereas the LTR group was impaired in
recalling the most recent ones (P3 and P4). Again, these
findings supported the importance of the right MTL
structures in the evocation of the episodic spatial context
of memories that consist of detailed perceptual–spatial
Brain (2007), 130, 3184 ^3199
3195
representations of experienced environments (Moscovitch
et al., 2005). The left MTL appears important in the evocation of more mundane memories, like those generally
retrieved for recent periods (Viard et al., 2007). The ‘when’
responses revealed that both RTR and LTR patients
produced fewer responses than normal control participants
for the remote periods (P1 and P2), whereas there was
no difference for the recent ones (P3 and P4). The role
of MTL structures has been emphasized in memory for
sequences of events (Fortin et al., 2002). In addition, the
integrity of those structures seems to be important in time
estimation, as indicated by several reports revealing a severe
distortion of temporal processing in amnesic patients with
bilateral MTL damage (Richards, 1973; Williams et al.,
1989). A recent study has also reported that patients
with either right or left unilateral MTL lesions were
impaired when estimating duration in the range of minutes
(Noulhiane et al., 2007). In agreement with these studies,
our results suggest that MTL structures are bilaterally
involved in processing of temporal attributes of events
(e.g. the date, the moment in the day or the duration of
the event). We found that the two patient groups were
impaired in remote periods although the LTR patients were
also affected in the most recent period (P4). Nevertheless,
given the lack of data in this domain, further studies will
be necessary to clarify the role of MTL structures in the
temporal attributes of episodic autobiographical memory.
Interestingly, the mixed findings obtained for the
temporal gradient question its operationalization in the
context of the two competing neurobiological models of
long-term episodic memory. Results of strictly episodic
autobiographical memories (SE) revealed that the control
group showed a recency effect, while the patients seemed to
show a ‘relative’ temporal gradient (i.e. greater impairment
in the recall of the recent as compared to previous periods),
although they performed below the control group regardless
of the time period. This result appears to be consistent
with the consolidation theory, which proposes differential
sparing of remote and recent memories (Squire and
Alvarez, 1995). However, the global impairment of patients
in all the time periods is compatible with the multi trace
theory (MTT) model (Nadel and Moscovitch, 1997, 2001;
Nadel and Hardt, 2004; Moscovitch et al., 2005) and
suggests that MTL structures are permanently involved in
the recall of episodic events. This latter interpretation
is further supported by the results observed with the (total)
remember responses given that the deficits of patients
tended to increase with remoteness. All these results
suggest that different cognitive processes are required
for memory of autobiographical events. The SE score is
based on the specific properties of narrative reports of
memories (uniqueness, spatiotemporal context and details),
whereas the remember responses focused on the subjective
feeling of remembering and the capacity to justify this
feeling. Therefore, the temporal gradient obtained with
the remember responses indicates that the judgments
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Brain (2007), 130, 3184 ^3199
of patients on their sense of remembering were more
reliable for the recent as compared to remote memories.
While our findings underline the complexity of relations
between the passage of time and the recall, they suggest that
our data may be more compatible with the MTT model
than the consolidation theory.
Concerning the issue of specific mechanisms (i.e. anterograde versus retrograde) involved in autobiographical
memory deficits, the results revealed that the patients
with left or right MTL resections were impaired in episodic
autobiographical memory as well as in autonoetic consciousness even for the early childhood period. Although it
is difficult to disentangle the anterograde and retrograde
mechanisms of deficits, it is plausible that some additional
anterograde deficits may have supplemented retrograde
ones in these patients. Indeed, the long-standing epileptic
disease associated with hippocampal sclerosis might have
disrupted the acquisition and consolidation of memories
acquired before the surgery, as the data reported by Kapur
and Prevett (2003) suggest. Such impairments would result
in a limited stock of accumulated knowledge about personal
events from childhood or adolescence. In our study,
however, as in most studies reported in the literature, we
were not able to demonstrate a relation between seizure
onset and different autobiographical memory scores. This
lack of correlation is consistent with previous findings
(Bergin et al., 2000; Viskontas et al., 2000; Lah et al., 2004;
Voltzenlogel et al., 2006). Viskontas and his colleagues for
example did not find significant differences in memory
scores when they compared early and late seizure onsets.
According to these authors, the absence of poorer performance in the early onset group weakens this conclusion,
although the possibility of defective encoding in both
groups cannot be discounted. The age of onset of ongoing
seizure disorders did not reflect the beginning of the
hippocampal sclerosis. The damage to MTL tissue probably
occurs during the latent period before experiencing
recurrent seizures. For instance, some studies have reported
that febrile seizures were preceded by changes in hippocampal morphology (Cavazos et al., 1994; Grunewald et al.,
2001). Lah et al. (2006) suggested that seizures themselves
may not only interfere with encoding and consolidation of
information, but also corrupt already established memory
stores. These authors also reported that young age of onset
(younger than 14 years) of temporal lobe epilepsy was
associated with greater difficulties in the subtest of recall of
famous events from ‘The Australian Remote Memory
Battery’. Nevertheless, this result was not observed in
the other subtests with the same patient groups (e.g. the
‘Autobiographical Fluency Test’). In our study, many
patients were younger than 14 years old at epilepsy onset.
Thus, it seems possible that an early encoding and
consolidation impairment could be partially responsible
for retrograde memory deficits in childhood and
adolescence.
M. Noulhiane et al.
Relationships between autobiographical
memory scores and volumetry of
temporal lobe structures
The correlation results suggest that unlike the lateral
temporal structures, MTL areas are involved in autobiographical memory, regardless of remoteness. They revealed
that for the most remote periods, the AM and total jR
scores involved the right parahippocampal cortex, which
is well known for its contribution to visual imagery and
spatial processing (Bohbot et al., 1998; O’Craven and
Kanwisher, 2000; Burgess et al., 2002; Ganis et al., 2004).
As suggested earlier, mental visual imagery and emotion
were particularly important in the retrieval of remote
memories (Rubin and Wetzler, 1986; Conway and Rubin,
1993; Fitzgerald, 1996; Rubin and Schulkind, 1997; Piolino
et al., 2002, 2007). Moreover, the most remote periods
included in the total jR score were also correlated with the
volume of the right temporopolar cortex; this might
be explained by its involvement in emotional processes
(Piefke et al., 2003) and retrieval of remote episodic
memories (Markowitsch, 1995; Conway, 2001). More
generally, these results may be considered to be in line
with neuroimaging data suggesting that right-sided MTL
activations are obtained during the retrieval of emotional
properties of autobiographical memories (Fink et al., 1996)
or of spatial details operating on the visual mental imagery,
which are especially relevant for remote autobiographical
memory ecphory (Mayes et al., 2000; Piolino et al., 2004).
For the most recent periods, the AM, SE and total jR
scores were correlated with the volume of the right
perirhinal cortex and the left hippocampus. The contribution of the right perirhinal cortex to recall of the most
recent periods could be related to the novelty of the
stimulus (Brown and Aggleton, 2001; Nyberg, 2005), while
those of the left hippocampus suggest its involvement in
associative novelty (Nyberg, 2005). Moreover, the finding
of left-sided involvement for recent periods may be in line
with the fact that memories from the most recent periods
(relative to more remote periods) are partly composed
of non-emotional events that had happened very recently
(a few days, weeks or months ago). Although such recent
memories are episodic in nature, they are unlikely to be
stored for the long term, unless they are highly goal-specific
and rehearsed (Conway, 2001). Our correlational and
regression results also support the multiple trace theory
model, which suggests that various MTL regions permanently contribute to the different aspects of either recent
or remote episodic autobiographical memory (Moscovitch
et al., 2005).
Overall, this study highlights the role of bilateral MTL
in episodic autobiographical memory independently of
remoteness, and suggests that the right MTL structures
are particularly responsive to the sense of reliving the
encoding context. Our findings are in keeping with neuroimaging studies detecting bilateral or preferential right MTL
Autobiographical memory after TLE surgery
activation when subjects are engaged in the retrieval of
specific autobiographical memories rated high for mental
imagery, richness of detail, emotionality, re-experiencing or
personal significance (Mayes et al., 2000; Ryan et al., 2001;
Graham et al., 2003; Piefke et al., 2003; Piolino et al., 2004;
Greenberg et al., 2005; Steinvorth et al., 2006; Viard et al.,
2007). Our results also confirm recent data indicating that
the qualities of retrieved memories influence the MTL
engagement independently of factors such as remoteness
(Graham et al., 2003; Addis et al., 2004; Gilboa et al., 2004;
Piolino et al., 2004; Viard et al., 2007). Moreover, they are
in accordance with Gilboa et al.’ s (2005) finding that there
is a significant correlation between remote autobiographical
memory in patients with brain lesions and the amount of
remaining tissue in bilateral MTL, which is stronger on the
right than the left. In our study, the major role of the right
MTL may be due to the fact that we specifically sought the
autonoetic qualities of autobiographical memories, such as
mental ‘time travel’ through subjective time, from the
present to the past, and re-experiencing, through selfawareness, one’s own previous experiences (Tulving, 2001).
Therefore, our results suggest that the right MTL
contributes to the successful retrieval of episodic memories
(e.g. from the reminiscence bump) that are greatly
dependent upon the richness of spatio-temporal details
and more specifically of phenomenal ones.
In conclusion, our results substantiate that patients with
left or right temporal lobe resections have impaired
episodic autobiographical memories. This impairment
concerns the entire lifespan including the early childhood
period and also affects autonoetic consciousness. Our
additional findings, based on correlation analysis, indicated
that this impairment was related to the medial rather than
the lateral temporal lobe structures. Our results suggest
that the right-hemisphere MTL structures are particularly
responsive to the sense of reliving the encoding context.
In agreement with the multi trace theory model, we found
that various MTL regions are permanently involved in
the different aspects of episodic autobiographical memory
(Moscovitch et al., 2005) in patients with unilateral
temporal lobe resection.
Acknowledgements
This work was supported by the French League Against
Epilepsy (Novartis to M.N.) and the Regional Council
of Nord Pas de Calais Picardie (Ph.D. fellowship to M.N.).
We thank Marie Chupin and Amee Baird for her helpful
technical assistance, Dr Gilles Huberfeld and Dr Johan
Pallud for their clinical expertise, Marisa Denos for the
neuropsychological assessment.
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