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Epilepsy & Behavior 21 (2011) 36–41

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Epilepsy & Behavior


j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h

Autobiographical memory and the self in a case of transient epileptic amnesia


Nathan A. Illman a,⁎, Clare J. Rathbone b, Steven Kemp c, Chris J.A. Moulin a
a
Institute of Psychological Sciences, University of Leeds, Leeds, UK
b
Department of Psychology, School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK
c
Department of Clinical and Health Psychology, St James’ Teaching Hospital, Leeds, UK

a r t i c l e i n f o a b s t r a c t

Article history: Transient epileptic amnesia (TEA) is characterized by deficits in autobiographical memory (AM). One of the
Received 29 November 2010 functions of AM is to maintain the self, suggesting that the self may undergo changes as a result of memory
Revised 31 January 2011 loss in temporal lobe epilepsy. To examine this, we used a modification of a task used to assess the relationship
Accepted 15 February 2011
between self and memory (the IAM task) in a single case, E.B. Despite complaints of AM loss, E.B. had no
Available online 8 April 2011
difficulty in producing a range of self-images (e.g., I am a husband) and collections of self-defining AMs in
Keywords:
support of these statements. E.B. produced fewer episodic memories at times of self-formation, but this did
Transient epileptic amnesia not seem to impact on the maintenance of self. The results support recent work suggesting the self may be
Recollection maintained in the absence of episodic memory. The application of tasks such as that used here will further
Episodic memory elucidate AM impairment in temporal lobe epilepsy.
Autobiographical memory © 2011 Elsevier Inc. All rights reserved.
Self
Identity

1. Introduction may predict that without the ability to experience ”me” in time, selfhood
would be diminished. Addis and Tippett [12] displayed evidence of
Subjective memory complaint in temporal lobe epilepsy (TLE) is this in Alzheimer's disease, where episodic memory impairment was
related to a significantly reduced quality of life (e.g., questionnaire related to a loss in the strength of identity, with patients producing
studies) [1,2]. Such studies overlook contemporary developments more abstract representations of the self than controls. However, other
in memory theory that pertain to the self. For instance, a recent studies in traumatic brain injury have revealed that in the absence of
development is that as well as deficits in anterograde learning, TLE intact episodic memory, the individual is still able to draw on semantic
is associated with varying degrees of remote or autobiographical knowledge to maintain a ”conceptual self ” [13]. This suggests that
memory (AM) impairment [3–5]. Because an intact AM system allows although the nature of self may be significantly altered, identity is not
one to reflect on one's personal past and project oneself into the future, necessarily lost in memory impairment.
it is essential for psychological well-being [6]. As such, researchers It is not yet known what the impact more subtle forms of AM
have tended to agree that one of the fundamental functions of AM is to impairment may have on identity in TLE. In the present study, we
maintain a coherent and stable sense of self over time [7,8]. To date, drew on recent cognitive experimental approaches to assessing the
there has been no explicit examination of the self and memory in self, and focused on a case of transient epileptic amnesia (TEA). TEA is
TLE. The focus of the current article is measurement of the complex characterized by subjective complaints of AM loss, in the absence of
relationship between self and memory in a case of TLE. any objectively measured anterograde deficit [4,14]. Episodic memory
Any assessment of AM and the self needs to take into account what impairment has been found to cover the entire life span in these
is known about its underlying processes and the phenomenology patients [15]. It is important to note that these deficits may be
associated with them. Neurocognitive theories make a critical distinc- somewhat more nebulous and subtle than the amnesia seen in head
tion between episodic and semantic memory [9,10]. Episodic memories injury or Alzheimer's disease as discussed above.
are accessed through ”mental time travel,” allowing us to reexperience It is subjective report that we focus on here. Episodic and semantic
sensory–perceptual affective details of an event [11]. This autonoetic memories give rise to different states of conscious awareness during
state of awareness gives rise to a personal sense of reliving the past. retrieval. We were interested to see how the subjective experience
In contrast, semantic memory is experienced as knowledge, without associated with self-defining memories of one's past would relate
details concerning acquisition of that information. Intuitively, then, one to aspects of identity. As such, we employed the remember/know
procedure, which asks participants to classify a retrieved memory
⁎ Corresponding author at: Institute of Psychological Sciences, University of Leeds,
as remembered, corresponding to a subjective quality of pastness
Leeds, UK, LS2 9JT. Fax: + 44 113 343 5749. and context, or known, corresponding to conceptual knowledge. We
E-mail address: n.a.illman05@leeds.ac.uk (N.A. Illman). reasoned that this first-person approach would allow a direct measure

1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.yebeh.2011.02.022
N.A. Illman et al. / Epilepsy & Behavior 21 (2011) 36–41 37

of ”phenomenological continuity.” which has been suggested to be and estimated premorbid IQ scores were also above average, as were
critical for maintenance of the self [16]. In brief, we present a detailed his scores on tests of executive function. This profile matches other
investigation of a typical case of TEA using a modification of the IAM documented cases of TEA, where standardized measures do not
memory task [8,13] that considers subjective states at retrieval and validate subjective memory complaints of patients.
the self in autobiographical memory. E.B.'s predominant complaint was that he had a loss of salient
autobiographical information from his retired life. Strikingly, he was
2. Case report: Patient E.B. unable to provide details of what his wife described as highly
memorable holidays to places such as New Zealand and Fiji. Moreover,
In February 2009, patient E.B., a right-handed 73-year-old man, he explained how his memories for remote events in general lacked
had a generalized tonic–clonic seizure lasting a couple of minutes, the vividness they once had.
arising from sleep. His right arm was possibly more rigid than his left.
He was taken to a hospital, and an ECG and blood tests were normal. 3. Method
The next day he had a brief vacant attack with gulping. After that he
could remember nothing of the events of the day. 3.1. Participants
E.B. and his caring wife described two other types of attacks going
back 20 years. They referred to “memory attacks” with sudden The comparison group consisted of 10 neurologically intact older
repetitive questioning. These lasted about 1–2 hours and, for a time, adults (4 male) matched with E.B. for age (M=71.9, SD=2.81). They
were thought to be transient global amnesia (TGA). More recently these were recruited from the older adult participant panel of Leeds Memory
attacks of amnesia lasted less than 1 hour and were associated with Group. The study was approved by the Institute of Psychological Sciences,
retrograde amnesia. Second, he experienced attacks of sudden nausea University of Leeds ethics committee, and adhered to the British
associated with a ”woozy feeling.“ Further, his wife reported involuntary Psychological Society's ethical principles.
gulping, chewing, and pallor, with these attacks lasting 5–10 minutes
and followed by fatigue. 3.2. Materials and procedure
Regarding past medical history, his birth was normal; he did not
have febrile convulsions and was never knocked out. He has been The IAM task is based on Kuhn and McPartland's [21] Twenty
treated for hypertension for many years and recently had treatment Statements Test (TST) and has shown that AMs cluster around the age
for benign prostatic hypertrophy. Neurological examination was at which various self-images emerge, demonstrating a quantifiable
normal, as were three EEGs, an MRI scan (head), and a PET scan. organizational role of the self in memory [8,13]. In the present study,
Levetiracetam (750 mg twice daily) was commenced and his seizures participants were sent two booklets to complete by post. In part 1,
went into remission. The neurological opinion was that E.B. presented the first page asked participants to generate 10 ”I am” statements,
with different manifestations of TLE, closely resembling Butler and which reflected stable and enduring self-images. Next, participants
colleagues’ [17] diagnostic criteria for TEA. selected the three self-images that were most important to them and
were asked to recall and write down 10 specific AMs to support
2.1. Subjective memory complaints and neuropsychological profile each self, giving each a brief title. For example, a supporting AM for the
self-image ”I am a father” might be ”taking my son to his first golf
E.B.'s neuropsychological investigation is summarized in Table 1. tournament.” The age at which the event occurred was then noted, and
E.B.'s standardized scores on the Wechsler Memory Scale, Third finally, participants gave an age of emergence for the three original ”I
Edition (WMS-III) [18], for immediate and delayed visual and verbal am's” (i.e., the age at which being a father was considered a stable
anterograde memory ranged from average to superior. His Full Scale aspect of identity). Self-images were dated after retrieval of supporting
memories so as not to influence which specific AMs were selected.
After this first booklet was returned, part 2 was compiled
Table 1
separately for each participant. Memories were transcribed and
Neuropsychological test results for E.B.
participants were instructed to reread their responses and carefully
Function Test E.B.'s score follow the instructions provided for the remember/know (R/K)
Premorbid intellectual WTAR 121 procedure [9,22], the Point of View paradigm [23], and rate rehearsal.
functioning For the R/K procedure, participants were asked to classify their
Intellectual ability WASI subjective state of awareness during retrieval: Participants were
Full Scale IQ 141
Learning and memory WMS-III
instructed to make a remember response for memories that conjured
Logical Memory I 15 internal thoughts, feelings, and sensory information from a specific
Faces I 12 event that lasted less than 1 day and was essentially ”relived” during
Verbal Paired Associates I 15 retrieval. They were asked to assign a know response to memories that
Letter Number Sequencing 13
lacked some of these contextual details, that may have been repeated
Spatial Span 16
Logical Memory II 16 events, and that did not conjure the same sensation of reliving the
Faces II 11 episode as a remember response. Finally, participants had the option
Verbal Paired Associates II 15 of choosing a guess response for memories that contained fragments
Rey Complex Figure of information they were not certain were true and more likely
Immediate 25.5
derived from other people's retelling of stories. The Point of View
Delayed 24
Executive function Categories completed paradigm focuses on the perspective experienced during retrieval.
Letter fluency (words/3 min) 66 Field (F) responses are assigned to memories in which recall was
Category fluency (words/3 ming) 49 experienced through the participant's own eyes, in a first-person
Trail Making
perspective; observer (O) responses are assigned to memories
Number sequencing 11
Letter sequencing 9 experienced in a third-person perspective. F and O perspectives
Number–letter switching 14 correspond to episodic and semantic memories similarly to R/K
Note. Age-scaled scores are in italics. WTAR, Wechsler Test of Adult Reading [19]; WASI,
judgments [24]. Rehearsal was reported on a scale of 1–7 for the level
Wechsler Abbreviated Scale of Intelligence [20]; WMS-III, Wechsler Memory Scale of rehearsal for that particular memory, with 1 indicating ”never think
Third Edition [18]. about it” and 7 indicating ”think about it all the time.”
38 N.A. Illman et al. / Epilepsy & Behavior 21 (2011) 36–41

4. Results on the associated age of self-emergence for that ”I am” statement.


Thus, each supporting memory was coded as number of years before
Our aim was to compare E.B. with the controls on their ability (negative) or after (positive) age of emergence. These data are
to produce specific AMs cued by a range of self-images. We were summarized in Fig. 2, and illustrate the formation of different self-
interested in the temporal distribution of these self-supporting images based on a distribution of AMs. For example, E.B.'s self image
memories and identity statements and the phenomenology associated ”I am very happily married“ was given an age of emergence of 23. One
with them. of his supporting memories for this was titled ”our first date,” which
E.B. produced 10 self-images, along with 30 memories to support occurred when he was 18. Therefore, the recoded score would be –5,
the 3 self-images he judged to be most significant: ”I am a granddad as this memory occurred 5 years before that self emerged.
and family man”; ”I am a Black Country man”; ”I am very happily The two experiments reported by Rathbone et al. [8] found that
married.” The supporting memories were later verified by E.B.'s wife. the majority of all participants’ supporting memories clustered in the
For controls, an average of 24.33 (SD = 7.78) memories were –4 to 5 epoch period, with more memories after the self emerged,
produced. In some circumstances, despite the instruction to provide than before it, recalled. As Fig. 2 displays, we have replicated this
specific memories, participants noted an age period spanning a finding in our comparison group. More than one-third of participants’
number of years, denoting a repeated event. In these cases, the supporting memories emerged within the –4 to 5 epoch, approxi-
midpoint of the age range was taken as the age of the memory for mately one-quarter of memories in the 6 to 15 epoch, and a decreasing
further analysis. For example, E.B. reported an “annual visit to the zoo” but relatively even distribution of memories for up to 30 years after
during the age range 10–16. In this case, the age used in further that. Our sample was, on average, about 20 years older than the mean
analyses was13 years. age of Rathbone and colleagues’ [8] subjects, and the average age of
emergence of self-images was considerably older here (22.9 vs 33.15).
4.1. Distribution of memories Therefore, our results suggest that as one ages, self-images continue to
emerge (such as being a grandparent), and people use AMs from later
First, we were interested to see if our older adult sample would life to support these images.
display the typical reminiscence bump, whereby the largest propor- E.B.'s distribution of memories follows a similar pattern, although he
tion of memories recalled are those between the ages of 10 and 30 produced more supporting AMs from before the age of self-emergence.
[25]. As Fig. 1 displays, the mean proportion of memories for controls This result is skewed, however, by the supporting memories for his self-
peaks in the period 11–20 years, with subsequent proportions image, “I am a Black Country man,” relating to his strong sense of
gradually decreasing throughout middle adulthood. This is followed belonging and identifying with his geographical upbringing in England.
by a very clear recency effect for the period 61–70, which is consistent His age of emergence for this was 26, but the majority of memories were
with other studies sampling AMs from older adults [26]. Whereas the generic repeated events that were given age ranges considerably before
control distribution is defined by two peaks, E.B.'s distribution is much the age of emergence. His inability to produce a number of specific
less consistent. Sixty percent of his memories come from between the episodic memories from this period is interesting, given that this
ages of 11 and 30, which is a much more prominent reminiscence identity seems particularly salient for E.B.
bump compared with controls. Following this, he is comparable to
controls in the proportion of memories coming from middle-aged 4.3. Subjective experience: Remember/Know and Point of View
periods, but he draws on far fewer memories from late-middle and
older age (51–70) to support his self-images. Therefore, on initial Thus far, the results indicate that E.B. is able to generate a number
observation, it would seem that this early period of life is particularly of AMs to support the formation of a range of self-images. Next, we
self-defining for E.B. aimed to assess if there was a qualitative difference in the nature
of those memories, measured by asking participants to report their
4.2. Age of emergence subjective state of consciousness during retrieval.
Table 2 lists the overall proportions of responses E.B. and controls
Having established the relative distribution of E.B.'s and the gave for R/K judgments and F/O judgments. When taking into account
controls’ self-supporting memories, we examined whether E.B. used the large variation in the controls’ responses, E.B. reported a level of R
AMs to support different selves in the same way as controls. Following
Rathbone et al. [8,13], each participant's memory was recoded based

Fig. 1. Proportion of self-supporting memories recalled across the life span for E.B. Fig. 2. Proportion of memories recalled from epochs around age of self-emergence in
versus mean proportion for controls (N = 10). IAM task.
N.A. Illman et al. / Epilepsy & Behavior 21 (2011) 36–41 39

Table 2
Proportion of responses associated with IAMs of E.B. and controls.

Remember/Know judgment Point of View

Remember Know Guess Field (F) Observer (O) F/O

E.B. 0.70 0.30 0.00 0.57 0.43 0.00


Control mean (SD) 0.78 (0.21) 0.20 (0.19) 0.02 (0.04) 0.80 (0.26) 0.16 (0.22) 0.04 (0.08)

and K responses for all memories comparable to that of the controls. (P N 0.05). Hence, a simple explanation involving individual differences
This initially suggests there is no difference in the number of memories in rehearsal cannot explain our above findings.
E.B. vividly recollects to support his self-images. For the Point of
View perspectives, however, he reported an equal amount of F and O
responses, whereas controls reported a large proportion of F 5. Discussion
responses. Moreover, E.B., to a greater extent than controls, reported
O perspective for a number of memories he assigned an R response. In In the present study, we aimed to assess how subjective impair-
controls, we see the expected pattern whereby R and K responses are ments in AM would affect the self in the context of TEA. We used the
generally assigned to field and observer perspectives, respectively IAM memory task, which explores the use of self-images to cue salient
[24].1 This, in itself, may be an indication that the subjective experience AMs. Our novel contribution to this literature was not only the first
associated with E.B.'s retrieval may lack some of the phenomenological empirical assessment of the self in a syndrome of TLE, but also a
detail encountered by adults similar in age to him. specific focus on the phenomenology associated with autobiographical
E.B. produced the majority of his supporting memories from the retrieval, reflecting the ”mental time travel” that is the hallmark of
period 11–20 years, suggesting this epoch is particularly self-defining episodic memory [9].
for him. Although previous research has also suggested this period In general, our results did not suggest that E.B. had a loss of self—he
represents the most personally significant time of self-formation in was able to produce 10 self-images and retrieved AMs that clustered
healthy adults [27], there have been few attempts to characterize around the age of emergence of the three most personally significant of
the subjective experience of associated memories. We therefore these. Moreover, the subjective experience ratings revealed that,
chose to compare E.B. and the controls with respect to the mean overall, E.B. appeared unimpaired in his ability to recollect specific
proportions for the subjective experience measures in this epoch. For episodes in support of his identity statements. On closer inspection,
controls, R, K, and G proportions were 0.74, 0.22, and 0.04, however, E.B. displayed a tendency to subjectively report two
respectively. E.B.'s respective proportions for R, K, and G judgments opposing states of consciousness during retrieval; he often reported
were 0.42 (z = –0.89), 0.58 (z = 1.44), and 0.00 (z = –1.00). In the recollecting an event despite retrieving the memory from a third-
same period, controls’ F, O, and both F and O judgments were 0.81, person perspective. Additionally, he almost solely relied on the use of
0.08, and 0.11, and E.B.'s were 0.33 (z = –1.30), 0.67 (z = 2.68), and semantic knowledge from his childhood and adolescence to support a
0.00 (z = –0.33), respectively. Given that the task instructions asked key identity, whereas controls were able to recollect detailed, episodic
for specific events that participants consider self-defining, one would information. Below we discuss some of the theoretical implications of
anticipate that these would be associated with a strong recollective these findings with respect to theories of the self and AM consolidation
component. The above data show that although E.B. generates most and suggest some potential clinical applications of the IAM task in TLE.
of his memories from this time period, they are associated with Our findings largely mirror those reported for P.J.M., a woman who
subjective states of awareness characteristic of semantic content. In had a traumatic brain injury resulting in dense retrograde amnesia
contrast, controls retrieve specific AMs, literally reliving the original [13]. The authors found that despite severe episodic memory deficits
context of the event. and a resulting inability to produce specific supporting memories, P.J.
M. drew on conceptual knowledge about her life to support the self.
Although our patient presented with comparatively milder AM
4.4. Rehearsal deficits when formally tested, we have shown a similar pattern of
results, suggesting that when episodic memories are unavailable, the
Because evidence suggests that repeated rehearsal of remote self is maintained through a reliance on semantic memory. This
memories may increase richness of their recollection [28], we assessed provides further evidence for the robustness of personal semantic
differences between E.B.'s and the controls’ subjectively rated memory in light of episodic impairments [30–33]. It also suggests that
rehearsal for each memory. A modified t test [29] revealed no even when there are deficits in the reexperiencing of the self at
significant difference between E.B. (2.20) and controls (M = 3.74, discrete moments in the past, or ”phenomenological continuity,” one
SD = 1.52) in overall average rehearsal scores (P N 0.05). In terms of age is still able to draw on an integrated and extended set of events to
of memory and level of rehearsal, small to moderate positive support a ”narrative continuity.” As Addis and Tippett describe, the
correlations were significant for both E.B. (r = 0.40, P = 0.03) and the relative importance of these processes is not yet well understood [12].
mean of the controls’ individual correlations (r = 0.29, P = 0.0001), What is particularly interesting is the fact that E.B. showed a
suggesting that the more recent the memory, the more it was preferential impairment in remembering memories from the remi-
rehearsed. Finally, because we found E.B. to have particular difficulty niscence bump, which is considered to reflect a period of salient self-
recollecting the most remote experiences, we compared his mean defining experiences [27]. Our evidence suggests that the retrieval of
rehearsal for memories up to 30 years old (2.05) with that of controls individual episodes that are experienced as vivid recollections from
(mean = 3.20, SD = 1.53) and again found no significant difference this time is not required for an intact self-representation, and that
collections of experiences may instead be used to the same end. In
support, in a study of 2341 healthy people aged 16–75, Janssen et al.
1
A nonparametric correlation was used to examine the association between R and K [34] showed that AMs were drawn predominantly from the ages of
and Point of View perspective in controls, G = 0.86, showing a robust relationship
between these two variables. For E.B., however, 19% of his memories given an R
6–20, but that memories from this period did not differ from those
response were with an observer perspective, whereas only 8% of responses were outside of this epoch in terms of self-rated vividness, or ”reliving”
assigned in this manner by controls. (the author's rating of recollection).
40 N.A. Illman et al. / Epilepsy & Behavior 21 (2011) 36–41

One cognitive theory of how the self is functionally supported Finally, as well as providing a novel way of assessing differences
comes from Klein et al. [35], who suggest that the transformation of a in memory pre- and postsurgery, the IAM task could also be used
memory trace into an autobiographical experience is reliant on self- to see how people's perceptions of themselves change throughout
reflection, self-agency, self-ownership, and personal temporality. the course of treatment, or any other chronic disease. This may be
The modified IAM task seems a particularly useful tool for assessing particularly instructive in cases where successful resective surgery
these dimensions: mentally reexperiencing or remembering past leads to a paradoxical difficulty in adjusting to ”normal” life, termed
events in their temporal order is dependent on self-reflection and the burden of normality [42,43].
temporality; and the ability to produce meaningful, idiosyncratic
self-images and conjure personal experiences as examples of those 6. Conclusions
requires agency and ownership. E.B.'s pattern of impairment then
can be incorporated into Klein and colleagues’ suggested approach of In summary, we found further support for the contribution of
identifying the resulting ”species” of amnesia as a function of the autobiographical memory to the self. In the absence of the subjective
relative breakdown of one or all of these processes. His impaired experience of remembering past, self-defining experiences, the
recollective experience suggests it is likely that he has combined self can remain stable and coherent through the use of conceptual
damage to both his capacity to self-reflect (required for autonoetic autobiographical knowledge. Our results provide further support for
awareness) and his ability to combine this with personal temporal- retrograde impairments in autobiographical memory observed
ity. Despite this, like P.J.M., he is able to chronologically order elsewhere in transient epileptic amnesia, and it is suggested that
semantic personal knowledge to form a coherent narrative of his past the clinical application of this measure to the general temporal lobe
and present. What we have shown in the present study is that even epilepsy population will be highly instructive, allowing a better
in the context of damage to one or more of these proposed processes, understanding of memory impairment and its impact on the self.
the self may remain intact. What is not known is whether people
with damage like E.B.'s are able to form new selves; this should be a
Acknowledgments
priority for future research. In other memory impairments a
”petrified” self is often observed [36], whereby memory deficits do
We are very grateful for the support of E.B. and his wife and for their
not permit the construction of new self-images.
comments on this article. This work was presented at the International
We propose that E.B. has a form of ”recollective retrograde amnesia,”
Congress on Epilepsy: Brain and Mind, Prague, March 2010.
in which chronic subclinical epileptiform activity has selectively
damaged hippocampus-based recollective processes. This would be
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