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Autobiographical memory and the self in a case of transient epileptic amnesia
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 b c
Institute of Psychological Sciences, University of Leeds, Leeds, UK Department of Psychology, School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK Department of Clinical and Health Psychology, St James’ Teaching Hospital, Leeds, UK
a r t i c l e
i n f o
Article history: Received 29 November 2010 Revised 31 January 2011 Accepted 15 February 2011 Available online 8 April 2011 Keywords: Transient epileptic amnesia Recollection Episodic memory Autobiographical memory Self Identity
a b s t r a c t Transient epileptic amnesia (TEA) is characterized by deficits in autobiographical memory (AM). One of the functions of AM is to maintain the self, suggesting that the self may undergo changes as a result of memory loss in temporal lobe epilepsy. To examine this, we used a modification of a task used to assess the relationship between self and memory (the IAM task) in a single case, E.B. Despite complaints of AM loss, E.B. had no difficulty in producing a range of self-images (e.g., I am a husband) and collections of self-defining AMs in support of these statements. E.B. produced fewer episodic memories at times of self-formation, but this did not seem to impact on the maintenance of self. The results support recent work suggesting the self may be maintained in the absence of episodic memory. The application of tasks such as that used here will further elucidate AM impairment in temporal lobe epilepsy. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Subjective memory complaint in temporal lobe epilepsy (TLE) is related to a significantly reduced quality of life (e.g., questionnaire studies) [1,2]. Such studies overlook contemporary developments in memory theory that pertain to the self. For instance, a recent development is that as well as deficits in anterograde learning, TLE is associated with varying degrees of remote or autobiographical memory (AM) impairment [3–5]. Because an intact AM system allows one to reflect on one's personal past and project oneself into the future, it is essential for psychological well-being [6]. As such, researchers have tended to agree that one of the fundamental functions of AM is to maintain a coherent and stable sense of self over time [7,8]. To date, there has been no explicit examination of the self and memory in TLE. The focus of the current article is measurement of the complex relationship between self and memory in a case of TLE. Any assessment of AM and the self needs to take into account what is known about its underlying processes and the phenomenology associated with them. Neurocognitive theories make a critical distinction between episodic and semantic memory [9,10]. Episodic memories are accessed through ”mental time travel,” allowing us to reexperience sensory–perceptual affective details of an event [11]. This autonoetic state of awareness gives rise to a personal sense of reliving the past. In contrast, semantic memory is experienced as knowledge, without details concerning acquisition of that information. Intuitively, then, one ⁎ Corresponding author at: Institute of Psychological Sciences, University of Leeds, Leeds, UK, LS2 9JT. Fax: + 44 113 343 5749. E-mail address: [email protected] (N.A. Illman). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.02.022
may predict that without the ability to experience ”me” in time, selfhood would be diminished. Addis and Tippett [12] displayed evidence of this in Alzheimer's disease, where episodic memory impairment was related to a loss in the strength of identity, with patients producing more abstract representations of the self than controls. However, other studies in traumatic brain injury have revealed that in the absence of intact episodic memory, the individual is still able to draw on semantic knowledge to maintain a ”conceptual self ” [13]. This suggests that although the nature of self may be significantly altered, identity is not necessarily lost in memory impairment. It is not yet known what the impact more subtle forms of AM impairment may have on identity in TLE. In the present study, we drew on recent cognitive experimental approaches to assessing the self, and focused on a case of transient epileptic amnesia (TEA). TEA is characterized by subjective complaints of AM loss, in the absence of any objectively measured anterograde deficit [4,14]. Episodic memory impairment has been found to cover the entire life span in these patients [15]. It is important to note that these deficits may be somewhat more nebulous and subtle than the amnesia seen in head injury or Alzheimer's disease as discussed above. It is subjective report that we focus on here. Episodic and semantic memories give rise to different states of conscious awareness during retrieval. We were interested to see how the subjective experience associated with self-defining memories of one's past would relate to aspects of identity. As such, we employed the remember/know procedure, which asks participants to classify a retrieved memory as remembered, corresponding to a subjective quality of pastness and context, or known, corresponding to conceptual knowledge. We reasoned that this first-person approach would allow a direct measure
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of ”phenomenological continuity.” which has been suggested to be critical for maintenance of the self [16]. In brief, we present a detailed investigation of a typical case of TEA using a modification of the IAM memory task [8,13] that considers subjective states at retrieval and the self in autobiographical memory. 2. Case report: Patient E.B. In February 2009, patient E.B., a right-handed 73-year-old man, had a generalized tonic–clonic seizure lasting a couple of minutes, 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. The next day he had a brief vacant attack with gulping. After that he could remember nothing of the events of the day. E.B. and his caring wife described two other types of attacks going back 20 years. They referred to “memory attacks” with sudden repetitive questioning. These lasted about 1–2 hours and, for a time, were thought to be transient global amnesia (TGA). More recently these attacks of amnesia lasted less than 1 hour and were associated with retrograde amnesia. Second, he experienced attacks of sudden nausea associated with a ”woozy feeling.“ Further, his wife reported involuntary gulping, chewing, and pallor, with these attacks lasting 5–10 minutes and followed by fatigue. Regarding past medical history, his birth was normal; he did not have febrile convulsions and was never knocked out. He has been treated for hypertension for many years and recently had treatment for benign prostatic hypertrophy. Neurological examination was normal, as were three EEGs, an MRI scan (head), and a PET scan. Levetiracetam (750 mg twice daily) was commenced and his seizures went into remission. The neurological opinion was that E.B. presented with different manifestations of TLE, closely resembling Butler and colleagues’ [17] diagnostic criteria for TEA. 2.1. Subjective memory complaints and neuropsychological profile E.B.'s neuropsychological investigation is summarized in Table 1. E.B.'s standardized scores on the Wechsler Memory Scale, Third Edition (WMS-III) [18], for immediate and delayed visual and verbal anterograde memory ranged from average to superior. His Full Scale
Table 1 Neuropsychological test results for E.B. Function
Test
E.B.'s score
Premorbid intellectual functioning Intellectual ability
WTAR
121
Learning and memory
Executive function
WASI Full Scale IQ WMS-III Logical Memory I Faces I Verbal Paired Associates I Letter Number Sequencing Spatial Span Logical Memory II Faces II Verbal Paired Associates II Rey Complex Figure Immediate Delayed Categories completed Letter fluency (words/3 min) Category fluency (words/3 ming) Trail Making Number sequencing Letter sequencing Number–letter switching
141 15 12 15 13 16 16 11 15 25.5 24 66 49 11 9 14
Note. Age-scaled scores are in italics. WTAR, Wechsler Test of Adult Reading [19]; WASI, Wechsler Abbreviated Scale of Intelligence [20]; WMS-III, Wechsler Memory Scale Third Edition [18].
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and estimated premorbid IQ scores were also above average, as were his scores on tests of executive function. This profile matches other documented cases of TEA, where standardized measures do not validate subjective memory complaints of patients. E.B.'s predominant complaint was that he had a loss of salient autobiographical information from his retired life. Strikingly, he was unable to provide details of what his wife described as highly memorable holidays to places such as New Zealand and Fiji. Moreover, he explained how his memories for remote events in general lacked the vividness they once had. 3. Method 3.1. Participants The comparison group consisted of 10 neurologically intact older adults (4 male) matched with E.B. for age (M=71.9, SD=2.81). They were recruited from the older adult participant panel of Leeds Memory Group. The study was approved by the Institute of Psychological Sciences, University of Leeds ethics committee, and adhered to the British Psychological Society's ethical principles. 3.2. Materials and procedure The IAM task is based on Kuhn and McPartland's [21] Twenty Statements Test (TST) and has shown that AMs cluster around the age at which various self-images emerge, demonstrating a quantifiable organizational role of the self in memory [8,13]. In the present study, participants were sent two booklets to complete by post. In part 1, the first page asked participants to generate 10 ”I am” statements, which reflected stable and enduring self-images. Next, participants selected the three self-images that were most important to them and were asked to recall and write down 10 specific AMs to support 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 tournament.” The age at which the event occurred was then noted, and finally, participants gave an age of emergence for the three original ”I am's” (i.e., the age at which being a father was considered a stable 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 separately for each participant. Memories were transcribed and participants were instructed to reread their responses and carefully follow the instructions provided for the remember/know (R/K) procedure [9,22], the Point of View paradigm [23], and rate rehearsal. For the R/K procedure, participants were asked to classify their subjective state of awareness during retrieval: Participants were instructed to make a remember response for memories that conjured internal thoughts, feelings, and sensory information from a specific event that lasted less than 1 day and was essentially ”relived” during retrieval. They were asked to assign a know response to memories that lacked some of these contextual details, that may have been repeated events, and that did not conjure the same sensation of reliving the episode as a remember response. Finally, participants had the option of choosing a guess response for memories that contained fragments of information they were not certain were true and more likely derived from other people's retelling of stories. The Point of View paradigm focuses on the perspective experienced during retrieval. Field (F) responses are assigned to memories in which recall was experienced through the participant's own eyes, in a first-person perspective; observer (O) responses are assigned to memories experienced in a third-person perspective. F and O perspectives correspond to episodic and semantic memories similarly to R/K judgments [24]. Rehearsal was reported on a scale of 1–7 for the level of rehearsal for that particular memory, with 1 indicating ”never think about it” and 7 indicating ”think about it all the time.”
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4. Results Our aim was to compare E.B. with the controls on their ability to produce specific AMs cued by a range of self-images. We were interested in the temporal distribution of these self-supporting memories and identity statements and the phenomenology associated with them. E.B. produced 10 self-images, along with 30 memories to support the 3 self-images he judged to be most significant: ”I am a granddad and family man”; ”I am a Black Country man”; ”I am very happily married.” The supporting memories were later verified by E.B.'s wife. For controls, an average of 24.33 (SD = 7.78) memories were produced. In some circumstances, despite the instruction to provide specific memories, participants noted an age period spanning a number of years, denoting a repeated event. In these cases, the midpoint of the age range was taken as the age of the memory for further analysis. For example, E.B. reported an “annual visit to the zoo” during the age range 10–16. In this case, the age used in further analyses was13 years. 4.1. Distribution of memories First, we were interested to see if our older adult sample would display the typical reminiscence bump, whereby the largest proportion of memories recalled are those between the ages of 10 and 30 [25]. As Fig. 1 displays, the mean proportion of memories for controls peaks in the period 11–20 years, with subsequent proportions gradually decreasing throughout middle adulthood. This is followed by a very clear recency effect for the period 61–70, which is consistent with other studies sampling AMs from older adults [26]. Whereas the control distribution is defined by two peaks, E.B.'s distribution is much less consistent. Sixty percent of his memories come from between the ages of 11 and 30, which is a much more prominent reminiscence bump compared with controls. Following this, he is comparable to controls in the proportion of memories coming from middle-aged periods, but he draws on far fewer memories from late-middle and older age (51–70) to support his self-images. Therefore, on initial observation, it would seem that this early period of life is particularly self-defining for E.B. 4.2. Age of emergence Having established the relative distribution of E.B.'s and the controls’ self-supporting memories, we examined whether E.B. used 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. versus mean proportion for controls (N = 10).
on the associated age of self-emergence for that ”I am” statement. Thus, each supporting memory was coded as number of years before (negative) or after (positive) age of emergence. These data are summarized in Fig. 2, and illustrate the formation of different selfimages based on a distribution of AMs. For example, E.B.'s self image ”I am very happily married“ was given an age of emergence of 23. One of his supporting memories for this was titled ”our first date,” which occurred when he was 18. Therefore, the recoded score would be –5, as this memory occurred 5 years before that self emerged. The two experiments reported by Rathbone et al. [8] found that the majority of all participants’ supporting memories clustered in the –4 to 5 epoch period, with more memories after the self emerged, than before it, recalled. As Fig. 2 displays, we have replicated this finding in our comparison group. More than one-third of participants’ supporting memories emerged within the –4 to 5 epoch, approximately one-quarter of memories in the 6 to 15 epoch, and a decreasing but relatively even distribution of memories for up to 30 years after that. Our sample was, on average, about 20 years older than the mean 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). Therefore, our results suggest that as one ages, self-images continue to emerge (such as being a grandparent), and people use AMs from later life to support these images. E.B.'s distribution of memories follows a similar pattern, although he produced more supporting AMs from before the age of self-emergence. This result is skewed, however, by the supporting memories for his selfimage, “I am a Black Country man,” relating to his strong sense of belonging and identifying with his geographical upbringing in England. His age of emergence for this was 26, but the majority of memories were generic repeated events that were given age ranges considerably before the age of emergence. His inability to produce a number of specific episodic memories from this period is interesting, given that this identity seems particularly salient for E.B. 4.3. Subjective experience: Remember/Know and Point of View Thus far, the results indicate that E.B. is able to generate a number of AMs to support the formation of a range of self-images. Next, we aimed to assess if there was a qualitative difference in the nature of those memories, measured by asking participants to report their subjective state of consciousness during retrieval. Table 2 lists the overall proportions of responses E.B. and controls gave for R/K judgments and F/O judgments. When taking into account the large variation in the controls’ responses, E.B. reported a level of R
Fig. 2. Proportion of memories recalled from epochs around age of self-emergence in IAM task.
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Table 2 Proportion of responses associated with IAMs of E.B. and controls. Remember/Know judgment
E.B. Control mean (SD)
Point of View
Remember
Know
Guess
Field (F)
Observer (O)
F/O
0.70 0.78 (0.21)
0.30 0.20 (0.19)
0.00 0.02 (0.04)
0.57 0.80 (0.26)
0.43 0.16 (0.22)
0.00 0.04 (0.08)
and K responses for all memories comparable to that of the controls. This initially suggests there is no difference in the number of memories 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 responses. Moreover, E.B., to a greater extent than controls, reported O perspective for a number of memories he assigned an R response. In controls, we see the expected pattern whereby R and K responses are generally assigned to field and observer perspectives, respectively [24].1 This, in itself, may be an indication that the subjective experience associated with E.B.'s retrieval may lack some of the phenomenological detail encountered by adults similar in age to him. E.B. produced the majority of his supporting memories from the period 11–20 years, suggesting this epoch is particularly self-defining for him. Although previous research has also suggested this period represents the most personally significant time of self-formation in healthy adults [27], there have been few attempts to characterize the subjective experience of associated memories. We therefore chose to compare E.B. and the controls with respect to the mean proportions for the subjective experience measures in this epoch. For controls, R, K, and G proportions were 0.74, 0.22, and 0.04, respectively. E.B.'s respective proportions for R, K, and G judgments were 0.42 (z = –0.89), 0.58 (z = 1.44), and 0.00 (z = –1.00). In the same period, controls’ F, O, and both F and O judgments were 0.81, 0.08, and 0.11, and E.B.'s were 0.33 (z = –1.30), 0.67 (z = 2.68), and 0.00 (z = –0.33), respectively. Given that the task instructions asked for specific events that participants consider self-defining, one would anticipate that these would be associated with a strong recollective component. The above data show that although E.B. generates most of his memories from this time period, they are associated with subjective states of awareness characteristic of semantic content. In contrast, controls retrieve specific AMs, literally reliving the original context of the event.
4.4. Rehearsal Because evidence suggests that repeated rehearsal of remote memories may increase richness of their recollection [28], we assessed differences between E.B.'s and the controls’ subjectively rated rehearsal for each memory. A modified t test [29] revealed no significant difference between E.B. (2.20) and controls (M = 3.74, SD = 1.52) in overall average rehearsal scores (P N 0.05). In terms of age of memory and level of rehearsal, small to moderate positive correlations were significant for both E.B. (r = 0.40, P = 0.03) and the mean of the controls’ individual correlations (r = 0.29, P = 0.0001), suggesting that the more recent the memory, the more it was rehearsed. Finally, because we found E.B. to have particular difficulty recollecting the most remote experiences, we compared his mean rehearsal for memories up to 30 years old (2.05) with that of controls (mean = 3.20, SD = 1.53) and again found no significant difference
1 A nonparametric correlation was used to examine the association between R and K 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 response were with an observer perspective, whereas only 8% of responses were assigned in this manner by controls.
(P N 0.05). Hence, a simple explanation involving individual differences in rehearsal cannot explain our above findings.
5. Discussion In the present study, we aimed to assess how subjective impairments in AM would affect the self in the context of TEA. We used the IAM memory task, which explores the use of self-images to cue salient AMs. Our novel contribution to this literature was not only the first empirical assessment of the self in a syndrome of TLE, but also a specific focus on the phenomenology associated with autobiographical retrieval, reflecting the ”mental time travel” that is the hallmark of episodic memory [9]. In general, our results did not suggest that E.B. had a loss of self—he was able to produce 10 self-images and retrieved AMs that clustered around the age of emergence of the three most personally significant of these. Moreover, the subjective experience ratings revealed that, overall, E.B. appeared unimpaired in his ability to recollect specific episodes in support of his identity statements. On closer inspection, however, E.B. displayed a tendency to subjectively report two opposing states of consciousness during retrieval; he often reported recollecting an event despite retrieving the memory from a thirdperson perspective. Additionally, he almost solely relied on the use of semantic knowledge from his childhood and adolescence to support a key identity, whereas controls were able to recollect detailed, episodic information. Below we discuss some of the theoretical implications of these findings with respect to theories of the self and AM consolidation and suggest some potential clinical applications of the IAM task in TLE. Our findings largely mirror those reported for P.J.M., a woman who had a traumatic brain injury resulting in dense retrograde amnesia [13]. The authors found that despite severe episodic memory deficits 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 deficits when formally tested, we have shown a similar pattern of results, suggesting that when episodic memories are unavailable, the self is maintained through a reliance on semantic memory. This provides further evidence for the robustness of personal semantic memory in light of episodic impairments [30–33]. It also suggests that even when there are deficits in the reexperiencing of the self at discrete moments in the past, or ”phenomenological continuity,” one is still able to draw on an integrated and extended set of events to support a ”narrative continuity.” As Addis and Tippett describe, the relative importance of these processes is not yet well understood [12]. What is particularly interesting is the fact that E.B. showed a preferential impairment in remembering memories from the reminiscence bump, which is considered to reflect a period of salient selfdefining experiences [27]. Our evidence suggests that the retrieval of individual episodes that are experienced as vivid recollections from 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. [34] showed that AMs were drawn predominantly from the ages of 6–20, but that memories from this period did not differ from those outside of this epoch in terms of self-rated vividness, or ”reliving” (the author's rating of recollection).
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One cognitive theory of how the self is functionally supported comes from Klein et al. [35], who suggest that the transformation of a memory trace into an autobiographical experience is reliant on selfreflection, self-agency, self-ownership, and personal temporality. The modified IAM task seems a particularly useful tool for assessing these dimensions: mentally reexperiencing or remembering past events in their temporal order is dependent on self-reflection and temporality; and the ability to produce meaningful, idiosyncratic self-images and conjure personal experiences as examples of those requires agency and ownership. E.B.'s pattern of impairment then can be incorporated into Klein and colleagues’ suggested approach of identifying the resulting ”species” of amnesia as a function of the relative breakdown of one or all of these processes. His impaired recollective experience suggests it is likely that he has combined damage to both his capacity to self-reflect (required for autonoetic awareness) and his ability to combine this with personal temporality. Despite this, like P.J.M., he is able to chronologically order semantic personal knowledge to form a coherent narrative of his past and present. What we have shown in the present study is that even in the context of damage to one or more of these proposed processes, 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 priority for future research. In other memory impairments a ”petrified” self is often observed [36], whereby memory deficits do not permit the construction of new self-images. We propose that E.B. has a form of ”recollective retrograde amnesia,” in which chronic subclinical epileptiform activity has selectively damaged hippocampus-based recollective processes. This would be consistent with evidence that TEA is associated with subtle hippocampal volume loss [37] and fits with current theories of the underlying neuropathological mechanism underlying this syndrome [e.g., 38]. The use of the IAM task in TLE and other neuropsychological populations is likely to inform this neurobiological debate further. For example, personal significance has been shown to modulate hippocampal activity [39], yet most typical AM tasks only ask for post hoc ratings of this measure. The IAM task explicitly requires generation of self-defining and personally significant experiences and, as shown in the present study, can record the subjective experience (and, hence, type of memory) associated with these. It therefore not only allows an exploration of the role of AM involvement in the self, but adds to the vastly expanding empirical literature on AM in general. Although we postulate that E.B. has a ”healthy” self, it would be interesting to see if current perceptions of identity are different when specific episodic memories are available, before the onset of his TEA. Such questions require longitudinal designs. The critical clinical issue here is that whereas E.B. spontaneously complained of memory loss, his standardized assessment did not identify any memory impairment. We propose that clinicians consider tests of AM and, at that, ones that examine subjective experience to better validate and explore memory impairment in the community of persons with epilepsy. To date, the neuropsychological application of the IAM task has been used in only single case work [13]. As a clinical tool, it quickly enables the clinician to focus on memories of some value to the patient, and there is an expected level of remembering for such memories. We would predict that other cases like E.B. would show intact clustering but impaired remembering on personally significant memories. Currently, patients’ perceptions of their illness are typically derived from questionnaires; the IAM task may be a useful adjunct to these by providing a rich source of information about how patients perceive the self and how impairments in AM may relate to this. Because of the high comorbidity of depression and anxiety in TLE [40,41], it would also be useful to assess differences in negative and positive self-images, particularly abstract trait-like identities pertaining to the self (e.g., “I am a worrier”) and associated memories, to better understand how depressed patients, for example, perceive their identity.
Finally, as well as providing a novel way of assessing differences in memory pre- and postsurgery, the IAM task could also be used to see how people's perceptions of themselves change throughout the course of treatment, or any other chronic disease. This may be particularly instructive in cases where successful resective surgery leads to a paradoxical difficulty in adjusting to ”normal” life, termed the burden of normality [42,43]. 6. Conclusions In summary, we found further support for the contribution of autobiographical memory to the self. In the absence of the subjective experience of remembering past, self-defining experiences, the self can remain stable and coherent through the use of conceptual autobiographical knowledge. Our results provide further support for retrograde impairments in autobiographical memory observed elsewhere in transient epileptic amnesia, and it is suggested that the clinical application of this measure to the general temporal lobe epilepsy population will be highly instructive, allowing a better understanding of memory impairment and its impact on the self. Acknowledgments We are very grateful for the support of E.B. and his wife and for their comments on this article. This work was presented at the International Congress on Epilepsy: Brain and Mind, Prague, March 2010. References [1] Fisher RS, Vickrey BG, Gibson P, et al. The impact of epilepsy from the patient's perspective: I. Descriptions and subjective perceptions. Epilepsy Res 2000;41:39–51. [2] Giovagnoli AR, Avanzini G. Quality of life and memory performance in patients with temporal lobe epilepsy. Acta Neurol Scand 2000;101:295–300. [3] Bell BD, Giovagnoli AR. Recent innovative studies of memory in temporal lobe epilepsy. Neuropsychol Rev 2007;17:455–76. [4] Butler CR, Zeman AZ. Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment. Brain 2008;131:2243–63. [5] Herfurth K, Kasper B, Schwarz M, Stefan H, Pauli E. Autobiographical memory in temporal lobe epilepsy: role of hippocampal and temporal lateral structures. Epilepsy Behav 2010;19:365–71. [6] Conway MA. Memory and the self. J Mem Lang 2005;53:594–628. [7] Bluck S. Autobiographical memory: exploring its functions in everyday life. Memory 2003;11:113–23. [8] Rathbone CJ, Moulin CJA, Conway MA. Self-centered memories: the reminiscence bump and the self. Mem Cogn 2008;36:1403–14. [9] Tulving E. Memory and consciousness. Can Psychol 1985;26:1–12. [10] Tulving E. Episodic memory: From mind to brain. Annu Rev Psychol 2002;53:1–25. [11] Conway MA. Sensory-perceptual episodic memory and its context: autobiographical memory. Philos Trans R Soc B 2001;356:1375–84. [12] Addis DR, Tippett LJ. Memory of myself: autobiographical memory and identity in Alzheimer's disease. Memory 2004;12:56–74. [13] Rathbone CJ, Moulin CJA, Conway MA. Autobiographical memory and amnesia: using conceptual knowledge to ground the self. NeuroCase 2009;15:405–18. [14] Zeman AZJ, Boniface SJ, Hodges JR. Transient epileptic amnesia: a description of the clinical and neuropsychological features in 10 cases and a review of the literature. J Neurol Neurosurg Psychiatry 1998;64:435–43. [15] Milton F, Muhlert N, Pindus DM, et al. Remote memory deficits in transient epileptic amnesia. Brain 2010;133:1368–79. [16] Addis DR, Tippett LJ. The contributions of autobiographical memory to the content and continuity of identity. In: Sani F, editor. Self-continuity: individual and collective perspectives. New York: Psychology Press; 2008. p. 71–84. [17] Butler CR, Graham KS, Hodges JR, Kapur N, Wardlaw JM, Zeman AZJ. The syndrome of transient epileptic amnesia. J Neurol Neurosurg Psychiatry 2007;78:208. [18] Wechsler D. Wechsler Memory Scale. 3rd ed. San Antonio, TX: Psychological Corp.; 1997. [19] WTAR: Wechsler Test of Adult Reading manual. San Antonio, TX: Psychological Corp.; 2001. [20] WASI: Wechsler Abbreviated Scale of Intelligence manual. San Antonio, TX: Psychological Corp.; 1999. [21] Kuhn MH, McPartland TS. An empirical investigation of self-attitudes. Am Sociol Rev 1954;19:68–76. [22] Gardiner JM, Ramponi C, Richardson-Klavehn A. Experiences of remembering, knowing, and guessing. Conscious Cogn 1998;7:1–26. [23] Nigro G, Neisser U. Point of view in personal memories. Cogn Psychol 1983;15:467–82. [24] Crawley SE, French CC. Field and observer viewpoint in remember–know memories of personal childhood events. Memory 2005;13:673–81.
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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 b c
Institute of Psychological Sciences, University of Leeds, Leeds, UK Department of Psychology, School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK Department of Clinical and Health Psychology, St James’ Teaching Hospital, Leeds, UK
a r t i c l e
i n f o
Article history: Received 29 November 2010 Revised 31 January 2011 Accepted 15 February 2011 Available online 8 April 2011 Keywords: Transient epileptic amnesia Recollection Episodic memory Autobiographical memory Self Identity
a b s t r a c t Transient epileptic amnesia (TEA) is characterized by deficits in autobiographical memory (AM). One of the functions of AM is to maintain the self, suggesting that the self may undergo changes as a result of memory loss in temporal lobe epilepsy. To examine this, we used a modification of a task used to assess the relationship between self and memory (the IAM task) in a single case, E.B. Despite complaints of AM loss, E.B. had no difficulty in producing a range of self-images (e.g., I am a husband) and collections of self-defining AMs in support of these statements. E.B. produced fewer episodic memories at times of self-formation, but this did not seem to impact on the maintenance of self. The results support recent work suggesting the self may be maintained in the absence of episodic memory. The application of tasks such as that used here will further elucidate AM impairment in temporal lobe epilepsy. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Subjective memory complaint in temporal lobe epilepsy (TLE) is related to a significantly reduced quality of life (e.g., questionnaire studies) [1,2]. Such studies overlook contemporary developments in memory theory that pertain to the self. For instance, a recent development is that as well as deficits in anterograde learning, TLE is associated with varying degrees of remote or autobiographical memory (AM) impairment [3–5]. Because an intact AM system allows one to reflect on one's personal past and project oneself into the future, it is essential for psychological well-being [6]. As such, researchers have tended to agree that one of the fundamental functions of AM is to maintain a coherent and stable sense of self over time [7,8]. To date, there has been no explicit examination of the self and memory in TLE. The focus of the current article is measurement of the complex relationship between self and memory in a case of TLE. Any assessment of AM and the self needs to take into account what is known about its underlying processes and the phenomenology associated with them. Neurocognitive theories make a critical distinction between episodic and semantic memory [9,10]. Episodic memories are accessed through ”mental time travel,” allowing us to reexperience sensory–perceptual affective details of an event [11]. This autonoetic state of awareness gives rise to a personal sense of reliving the past. In contrast, semantic memory is experienced as knowledge, without details concerning acquisition of that information. Intuitively, then, one ⁎ Corresponding author at: Institute of Psychological Sciences, University of Leeds, Leeds, UK, LS2 9JT. Fax: + 44 113 343 5749. E-mail address: [email protected] (N.A. Illman). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.02.022
may predict that without the ability to experience ”me” in time, selfhood would be diminished. Addis and Tippett [12] displayed evidence of this in Alzheimer's disease, where episodic memory impairment was related to a loss in the strength of identity, with patients producing more abstract representations of the self than controls. However, other studies in traumatic brain injury have revealed that in the absence of intact episodic memory, the individual is still able to draw on semantic knowledge to maintain a ”conceptual self ” [13]. This suggests that although the nature of self may be significantly altered, identity is not necessarily lost in memory impairment. It is not yet known what the impact more subtle forms of AM impairment may have on identity in TLE. In the present study, we drew on recent cognitive experimental approaches to assessing the self, and focused on a case of transient epileptic amnesia (TEA). TEA is characterized by subjective complaints of AM loss, in the absence of any objectively measured anterograde deficit [4,14]. Episodic memory impairment has been found to cover the entire life span in these patients [15]. It is important to note that these deficits may be somewhat more nebulous and subtle than the amnesia seen in head injury or Alzheimer's disease as discussed above. It is subjective report that we focus on here. Episodic and semantic memories give rise to different states of conscious awareness during retrieval. We were interested to see how the subjective experience associated with self-defining memories of one's past would relate to aspects of identity. As such, we employed the remember/know procedure, which asks participants to classify a retrieved memory as remembered, corresponding to a subjective quality of pastness and context, or known, corresponding to conceptual knowledge. We reasoned that this first-person approach would allow a direct measure
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of ”phenomenological continuity.” which has been suggested to be critical for maintenance of the self [16]. In brief, we present a detailed investigation of a typical case of TEA using a modification of the IAM memory task [8,13] that considers subjective states at retrieval and the self in autobiographical memory. 2. Case report: Patient E.B. In February 2009, patient E.B., a right-handed 73-year-old man, had a generalized tonic–clonic seizure lasting a couple of minutes, 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. The next day he had a brief vacant attack with gulping. After that he could remember nothing of the events of the day. E.B. and his caring wife described two other types of attacks going back 20 years. They referred to “memory attacks” with sudden repetitive questioning. These lasted about 1–2 hours and, for a time, were thought to be transient global amnesia (TGA). More recently these attacks of amnesia lasted less than 1 hour and were associated with retrograde amnesia. Second, he experienced attacks of sudden nausea associated with a ”woozy feeling.“ Further, his wife reported involuntary gulping, chewing, and pallor, with these attacks lasting 5–10 minutes and followed by fatigue. Regarding past medical history, his birth was normal; he did not have febrile convulsions and was never knocked out. He has been treated for hypertension for many years and recently had treatment for benign prostatic hypertrophy. Neurological examination was normal, as were three EEGs, an MRI scan (head), and a PET scan. Levetiracetam (750 mg twice daily) was commenced and his seizures went into remission. The neurological opinion was that E.B. presented with different manifestations of TLE, closely resembling Butler and colleagues’ [17] diagnostic criteria for TEA. 2.1. Subjective memory complaints and neuropsychological profile E.B.'s neuropsychological investigation is summarized in Table 1. E.B.'s standardized scores on the Wechsler Memory Scale, Third Edition (WMS-III) [18], for immediate and delayed visual and verbal anterograde memory ranged from average to superior. His Full Scale
Table 1 Neuropsychological test results for E.B. Function
Test
E.B.'s score
Premorbid intellectual functioning Intellectual ability
WTAR
121
Learning and memory
Executive function
WASI Full Scale IQ WMS-III Logical Memory I Faces I Verbal Paired Associates I Letter Number Sequencing Spatial Span Logical Memory II Faces II Verbal Paired Associates II Rey Complex Figure Immediate Delayed Categories completed Letter fluency (words/3 min) Category fluency (words/3 ming) Trail Making Number sequencing Letter sequencing Number–letter switching
141 15 12 15 13 16 16 11 15 25.5 24 66 49 11 9 14
Note. Age-scaled scores are in italics. WTAR, Wechsler Test of Adult Reading [19]; WASI, Wechsler Abbreviated Scale of Intelligence [20]; WMS-III, Wechsler Memory Scale Third Edition [18].
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and estimated premorbid IQ scores were also above average, as were his scores on tests of executive function. This profile matches other documented cases of TEA, where standardized measures do not validate subjective memory complaints of patients. E.B.'s predominant complaint was that he had a loss of salient autobiographical information from his retired life. Strikingly, he was unable to provide details of what his wife described as highly memorable holidays to places such as New Zealand and Fiji. Moreover, he explained how his memories for remote events in general lacked the vividness they once had. 3. Method 3.1. Participants The comparison group consisted of 10 neurologically intact older adults (4 male) matched with E.B. for age (M=71.9, SD=2.81). They were recruited from the older adult participant panel of Leeds Memory Group. The study was approved by the Institute of Psychological Sciences, University of Leeds ethics committee, and adhered to the British Psychological Society's ethical principles. 3.2. Materials and procedure The IAM task is based on Kuhn and McPartland's [21] Twenty Statements Test (TST) and has shown that AMs cluster around the age at which various self-images emerge, demonstrating a quantifiable organizational role of the self in memory [8,13]. In the present study, participants were sent two booklets to complete by post. In part 1, the first page asked participants to generate 10 ”I am” statements, which reflected stable and enduring self-images. Next, participants selected the three self-images that were most important to them and were asked to recall and write down 10 specific AMs to support 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 tournament.” The age at which the event occurred was then noted, and finally, participants gave an age of emergence for the three original ”I am's” (i.e., the age at which being a father was considered a stable 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 separately for each participant. Memories were transcribed and participants were instructed to reread their responses and carefully follow the instructions provided for the remember/know (R/K) procedure [9,22], the Point of View paradigm [23], and rate rehearsal. For the R/K procedure, participants were asked to classify their subjective state of awareness during retrieval: Participants were instructed to make a remember response for memories that conjured internal thoughts, feelings, and sensory information from a specific event that lasted less than 1 day and was essentially ”relived” during retrieval. They were asked to assign a know response to memories that lacked some of these contextual details, that may have been repeated events, and that did not conjure the same sensation of reliving the episode as a remember response. Finally, participants had the option of choosing a guess response for memories that contained fragments of information they were not certain were true and more likely derived from other people's retelling of stories. The Point of View paradigm focuses on the perspective experienced during retrieval. Field (F) responses are assigned to memories in which recall was experienced through the participant's own eyes, in a first-person perspective; observer (O) responses are assigned to memories experienced in a third-person perspective. F and O perspectives correspond to episodic and semantic memories similarly to R/K judgments [24]. Rehearsal was reported on a scale of 1–7 for the level of rehearsal for that particular memory, with 1 indicating ”never think about it” and 7 indicating ”think about it all the time.”
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4. Results Our aim was to compare E.B. with the controls on their ability to produce specific AMs cued by a range of self-images. We were interested in the temporal distribution of these self-supporting memories and identity statements and the phenomenology associated with them. E.B. produced 10 self-images, along with 30 memories to support the 3 self-images he judged to be most significant: ”I am a granddad and family man”; ”I am a Black Country man”; ”I am very happily married.” The supporting memories were later verified by E.B.'s wife. For controls, an average of 24.33 (SD = 7.78) memories were produced. In some circumstances, despite the instruction to provide specific memories, participants noted an age period spanning a number of years, denoting a repeated event. In these cases, the midpoint of the age range was taken as the age of the memory for further analysis. For example, E.B. reported an “annual visit to the zoo” during the age range 10–16. In this case, the age used in further analyses was13 years. 4.1. Distribution of memories First, we were interested to see if our older adult sample would display the typical reminiscence bump, whereby the largest proportion of memories recalled are those between the ages of 10 and 30 [25]. As Fig. 1 displays, the mean proportion of memories for controls peaks in the period 11–20 years, with subsequent proportions gradually decreasing throughout middle adulthood. This is followed by a very clear recency effect for the period 61–70, which is consistent with other studies sampling AMs from older adults [26]. Whereas the control distribution is defined by two peaks, E.B.'s distribution is much less consistent. Sixty percent of his memories come from between the ages of 11 and 30, which is a much more prominent reminiscence bump compared with controls. Following this, he is comparable to controls in the proportion of memories coming from middle-aged periods, but he draws on far fewer memories from late-middle and older age (51–70) to support his self-images. Therefore, on initial observation, it would seem that this early period of life is particularly self-defining for E.B. 4.2. Age of emergence Having established the relative distribution of E.B.'s and the controls’ self-supporting memories, we examined whether E.B. used 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. versus mean proportion for controls (N = 10).
on the associated age of self-emergence for that ”I am” statement. Thus, each supporting memory was coded as number of years before (negative) or after (positive) age of emergence. These data are summarized in Fig. 2, and illustrate the formation of different selfimages based on a distribution of AMs. For example, E.B.'s self image ”I am very happily married“ was given an age of emergence of 23. One of his supporting memories for this was titled ”our first date,” which occurred when he was 18. Therefore, the recoded score would be –5, as this memory occurred 5 years before that self emerged. The two experiments reported by Rathbone et al. [8] found that the majority of all participants’ supporting memories clustered in the –4 to 5 epoch period, with more memories after the self emerged, than before it, recalled. As Fig. 2 displays, we have replicated this finding in our comparison group. More than one-third of participants’ supporting memories emerged within the –4 to 5 epoch, approximately one-quarter of memories in the 6 to 15 epoch, and a decreasing but relatively even distribution of memories for up to 30 years after that. Our sample was, on average, about 20 years older than the mean 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). Therefore, our results suggest that as one ages, self-images continue to emerge (such as being a grandparent), and people use AMs from later life to support these images. E.B.'s distribution of memories follows a similar pattern, although he produced more supporting AMs from before the age of self-emergence. This result is skewed, however, by the supporting memories for his selfimage, “I am a Black Country man,” relating to his strong sense of belonging and identifying with his geographical upbringing in England. His age of emergence for this was 26, but the majority of memories were generic repeated events that were given age ranges considerably before the age of emergence. His inability to produce a number of specific episodic memories from this period is interesting, given that this identity seems particularly salient for E.B. 4.3. Subjective experience: Remember/Know and Point of View Thus far, the results indicate that E.B. is able to generate a number of AMs to support the formation of a range of self-images. Next, we aimed to assess if there was a qualitative difference in the nature of those memories, measured by asking participants to report their subjective state of consciousness during retrieval. Table 2 lists the overall proportions of responses E.B. and controls gave for R/K judgments and F/O judgments. When taking into account the large variation in the controls’ responses, E.B. reported a level of R
Fig. 2. Proportion of memories recalled from epochs around age of self-emergence in IAM task.
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Table 2 Proportion of responses associated with IAMs of E.B. and controls. Remember/Know judgment
E.B. Control mean (SD)
Point of View
Remember
Know
Guess
Field (F)
Observer (O)
F/O
0.70 0.78 (0.21)
0.30 0.20 (0.19)
0.00 0.02 (0.04)
0.57 0.80 (0.26)
0.43 0.16 (0.22)
0.00 0.04 (0.08)
and K responses for all memories comparable to that of the controls. This initially suggests there is no difference in the number of memories 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 responses. Moreover, E.B., to a greater extent than controls, reported O perspective for a number of memories he assigned an R response. In controls, we see the expected pattern whereby R and K responses are generally assigned to field and observer perspectives, respectively [24].1 This, in itself, may be an indication that the subjective experience associated with E.B.'s retrieval may lack some of the phenomenological detail encountered by adults similar in age to him. E.B. produced the majority of his supporting memories from the period 11–20 years, suggesting this epoch is particularly self-defining for him. Although previous research has also suggested this period represents the most personally significant time of self-formation in healthy adults [27], there have been few attempts to characterize the subjective experience of associated memories. We therefore chose to compare E.B. and the controls with respect to the mean proportions for the subjective experience measures in this epoch. For controls, R, K, and G proportions were 0.74, 0.22, and 0.04, respectively. E.B.'s respective proportions for R, K, and G judgments were 0.42 (z = –0.89), 0.58 (z = 1.44), and 0.00 (z = –1.00). In the same period, controls’ F, O, and both F and O judgments were 0.81, 0.08, and 0.11, and E.B.'s were 0.33 (z = –1.30), 0.67 (z = 2.68), and 0.00 (z = –0.33), respectively. Given that the task instructions asked for specific events that participants consider self-defining, one would anticipate that these would be associated with a strong recollective component. The above data show that although E.B. generates most of his memories from this time period, they are associated with subjective states of awareness characteristic of semantic content. In contrast, controls retrieve specific AMs, literally reliving the original context of the event.
4.4. Rehearsal Because evidence suggests that repeated rehearsal of remote memories may increase richness of their recollection [28], we assessed differences between E.B.'s and the controls’ subjectively rated rehearsal for each memory. A modified t test [29] revealed no significant difference between E.B. (2.20) and controls (M = 3.74, SD = 1.52) in overall average rehearsal scores (P N 0.05). In terms of age of memory and level of rehearsal, small to moderate positive correlations were significant for both E.B. (r = 0.40, P = 0.03) and the mean of the controls’ individual correlations (r = 0.29, P = 0.0001), suggesting that the more recent the memory, the more it was rehearsed. Finally, because we found E.B. to have particular difficulty recollecting the most remote experiences, we compared his mean rehearsal for memories up to 30 years old (2.05) with that of controls (mean = 3.20, SD = 1.53) and again found no significant difference
1 A nonparametric correlation was used to examine the association between R and K 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 response were with an observer perspective, whereas only 8% of responses were assigned in this manner by controls.
(P N 0.05). Hence, a simple explanation involving individual differences in rehearsal cannot explain our above findings.
5. Discussion In the present study, we aimed to assess how subjective impairments in AM would affect the self in the context of TEA. We used the IAM memory task, which explores the use of self-images to cue salient AMs. Our novel contribution to this literature was not only the first empirical assessment of the self in a syndrome of TLE, but also a specific focus on the phenomenology associated with autobiographical retrieval, reflecting the ”mental time travel” that is the hallmark of episodic memory [9]. In general, our results did not suggest that E.B. had a loss of self—he was able to produce 10 self-images and retrieved AMs that clustered around the age of emergence of the three most personally significant of these. Moreover, the subjective experience ratings revealed that, overall, E.B. appeared unimpaired in his ability to recollect specific episodes in support of his identity statements. On closer inspection, however, E.B. displayed a tendency to subjectively report two opposing states of consciousness during retrieval; he often reported recollecting an event despite retrieving the memory from a thirdperson perspective. Additionally, he almost solely relied on the use of semantic knowledge from his childhood and adolescence to support a key identity, whereas controls were able to recollect detailed, episodic information. Below we discuss some of the theoretical implications of these findings with respect to theories of the self and AM consolidation and suggest some potential clinical applications of the IAM task in TLE. Our findings largely mirror those reported for P.J.M., a woman who had a traumatic brain injury resulting in dense retrograde amnesia [13]. The authors found that despite severe episodic memory deficits 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 deficits when formally tested, we have shown a similar pattern of results, suggesting that when episodic memories are unavailable, the self is maintained through a reliance on semantic memory. This provides further evidence for the robustness of personal semantic memory in light of episodic impairments [30–33]. It also suggests that even when there are deficits in the reexperiencing of the self at discrete moments in the past, or ”phenomenological continuity,” one is still able to draw on an integrated and extended set of events to support a ”narrative continuity.” As Addis and Tippett describe, the relative importance of these processes is not yet well understood [12]. What is particularly interesting is the fact that E.B. showed a preferential impairment in remembering memories from the reminiscence bump, which is considered to reflect a period of salient selfdefining experiences [27]. Our evidence suggests that the retrieval of individual episodes that are experienced as vivid recollections from 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. [34] showed that AMs were drawn predominantly from the ages of 6–20, but that memories from this period did not differ from those outside of this epoch in terms of self-rated vividness, or ”reliving” (the author's rating of recollection).
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One cognitive theory of how the self is functionally supported comes from Klein et al. [35], who suggest that the transformation of a memory trace into an autobiographical experience is reliant on selfreflection, self-agency, self-ownership, and personal temporality. The modified IAM task seems a particularly useful tool for assessing these dimensions: mentally reexperiencing or remembering past events in their temporal order is dependent on self-reflection and temporality; and the ability to produce meaningful, idiosyncratic self-images and conjure personal experiences as examples of those requires agency and ownership. E.B.'s pattern of impairment then can be incorporated into Klein and colleagues’ suggested approach of identifying the resulting ”species” of amnesia as a function of the relative breakdown of one or all of these processes. His impaired recollective experience suggests it is likely that he has combined damage to both his capacity to self-reflect (required for autonoetic awareness) and his ability to combine this with personal temporality. Despite this, like P.J.M., he is able to chronologically order semantic personal knowledge to form a coherent narrative of his past and present. What we have shown in the present study is that even in the context of damage to one or more of these proposed processes, 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 priority for future research. In other memory impairments a ”petrified” self is often observed [36], whereby memory deficits do not permit the construction of new self-images. We propose that E.B. has a form of ”recollective retrograde amnesia,” in which chronic subclinical epileptiform activity has selectively damaged hippocampus-based recollective processes. This would be consistent with evidence that TEA is associated with subtle hippocampal volume loss [37] and fits with current theories of the underlying neuropathological mechanism underlying this syndrome [e.g., 38]. The use of the IAM task in TLE and other neuropsychological populations is likely to inform this neurobiological debate further. For example, personal significance has been shown to modulate hippocampal activity [39], yet most typical AM tasks only ask for post hoc ratings of this measure. The IAM task explicitly requires generation of self-defining and personally significant experiences and, as shown in the present study, can record the subjective experience (and, hence, type of memory) associated with these. It therefore not only allows an exploration of the role of AM involvement in the self, but adds to the vastly expanding empirical literature on AM in general. Although we postulate that E.B. has a ”healthy” self, it would be interesting to see if current perceptions of identity are different when specific episodic memories are available, before the onset of his TEA. Such questions require longitudinal designs. The critical clinical issue here is that whereas E.B. spontaneously complained of memory loss, his standardized assessment did not identify any memory impairment. We propose that clinicians consider tests of AM and, at that, ones that examine subjective experience to better validate and explore memory impairment in the community of persons with epilepsy. To date, the neuropsychological application of the IAM task has been used in only single case work [13]. As a clinical tool, it quickly enables the clinician to focus on memories of some value to the patient, and there is an expected level of remembering for such memories. We would predict that other cases like E.B. would show intact clustering but impaired remembering on personally significant memories. Currently, patients’ perceptions of their illness are typically derived from questionnaires; the IAM task may be a useful adjunct to these by providing a rich source of information about how patients perceive the self and how impairments in AM may relate to this. Because of the high comorbidity of depression and anxiety in TLE [40,41], it would also be useful to assess differences in negative and positive self-images, particularly abstract trait-like identities pertaining to the self (e.g., “I am a worrier”) and associated memories, to better understand how depressed patients, for example, perceive their identity.
Finally, as well as providing a novel way of assessing differences in memory pre- and postsurgery, the IAM task could also be used to see how people's perceptions of themselves change throughout the course of treatment, or any other chronic disease. This may be particularly instructive in cases where successful resective surgery leads to a paradoxical difficulty in adjusting to ”normal” life, termed the burden of normality [42,43]. 6. Conclusions In summary, we found further support for the contribution of autobiographical memory to the self. In the absence of the subjective experience of remembering past, self-defining experiences, the self can remain stable and coherent through the use of conceptual autobiographical knowledge. Our results provide further support for retrograde impairments in autobiographical memory observed elsewhere in transient epileptic amnesia, and it is suggested that the clinical application of this measure to the general temporal lobe epilepsy population will be highly instructive, allowing a better understanding of memory impairment and its impact on the self. Acknowledgments We are very grateful for the support of E.B. and his wife and for their comments on this article. This work was presented at the International Congress on Epilepsy: Brain and Mind, Prague, March 2010. References [1] Fisher RS, Vickrey BG, Gibson P, et al. The impact of epilepsy from the patient's perspective: I. Descriptions and subjective perceptions. Epilepsy Res 2000;41:39–51. [2] Giovagnoli AR, Avanzini G. Quality of life and memory performance in patients with temporal lobe epilepsy. Acta Neurol Scand 2000;101:295–300. [3] Bell BD, Giovagnoli AR. Recent innovative studies of memory in temporal lobe epilepsy. Neuropsychol Rev 2007;17:455–76. [4] Butler CR, Zeman AZ. Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment. Brain 2008;131:2243–63. [5] Herfurth K, Kasper B, Schwarz M, Stefan H, Pauli E. Autobiographical memory in temporal lobe epilepsy: role of hippocampal and temporal lateral structures. Epilepsy Behav 2010;19:365–71. [6] Conway MA. Memory and the self. J Mem Lang 2005;53:594–628. [7] Bluck S. Autobiographical memory: exploring its functions in everyday life. Memory 2003;11:113–23. [8] Rathbone CJ, Moulin CJA, Conway MA. Self-centered memories: the reminiscence bump and the self. Mem Cogn 2008;36:1403–14. [9] Tulving E. Memory and consciousness. Can Psychol 1985;26:1–12. [10] Tulving E. Episodic memory: From mind to brain. Annu Rev Psychol 2002;53:1–25. [11] Conway MA. Sensory-perceptual episodic memory and its context: autobiographical memory. Philos Trans R Soc B 2001;356:1375–84. [12] Addis DR, Tippett LJ. Memory of myself: autobiographical memory and identity in Alzheimer's disease. Memory 2004;12:56–74. [13] Rathbone CJ, Moulin CJA, Conway MA. Autobiographical memory and amnesia: using conceptual knowledge to ground the self. NeuroCase 2009;15:405–18. [14] Zeman AZJ, Boniface SJ, Hodges JR. Transient epileptic amnesia: a description of the clinical and neuropsychological features in 10 cases and a review of the literature. J Neurol Neurosurg Psychiatry 1998;64:435–43. [15] Milton F, Muhlert N, Pindus DM, et al. Remote memory deficits in transient epileptic amnesia. Brain 2010;133:1368–79. [16] Addis DR, Tippett LJ. The contributions of autobiographical memory to the content and continuity of identity. In: Sani F, editor. Self-continuity: individual and collective perspectives. New York: Psychology Press; 2008. p. 71–84. [17] Butler CR, Graham KS, Hodges JR, Kapur N, Wardlaw JM, Zeman AZJ. The syndrome of transient epileptic amnesia. J Neurol Neurosurg Psychiatry 2007;78:208. [18] Wechsler D. Wechsler Memory Scale. 3rd ed. San Antonio, TX: Psychological Corp.; 1997. [19] WTAR: Wechsler Test of Adult Reading manual. San Antonio, TX: Psychological Corp.; 2001. [20] WASI: Wechsler Abbreviated Scale of Intelligence manual. San Antonio, TX: Psychological Corp.; 1999. [21] Kuhn MH, McPartland TS. An empirical investigation of self-attitudes. Am Sociol Rev 1954;19:68–76. [22] Gardiner JM, Ramponi C, Richardson-Klavehn A. Experiences of remembering, knowing, and guessing. Conscious Cogn 1998;7:1–26. [23] Nigro G, Neisser U. Point of view in personal memories. Cogn Psychol 1983;15:467–82. [24] Crawley SE, French CC. Field and observer viewpoint in remember–know memories of personal childhood events. Memory 2005;13:673–81.
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