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cortex 45 (2009) 566–574

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Research report ‘‘Do you remember what you did on March 13, 1985?’’ A case study of confabulatory hypermnesia

Gianfranco Dalla Barbaa,b,c,d,* and Caroline Decaixe aInserm U. 610, Paris, France bUniversite´ Pierre et Marie Curie-Paris 6, Paris, France cAP-HP, Hoˆpital Henri Mondor, Service de Neurologie, Cre´teil, France dDipartimento di Psicologia, Universita` di Trieste, Trieste, Italy eAP-HP, Hoˆpital Saint Antoine, Service de Neurologie, Paris, France article info abstract

Article history: We report on a patient, LM, with a Korsakoff’s syndrome who showed the unusual ten- Received 8 March 2007 dency to consistently provide a confabulatory answer to episodic questions for Reviewed 25 May 2007 which the predicted and most frequently observed response in normal subjects and in con- Revised 7 January 2008 fabulators is ‘‘I don’t know’’. LM’s pattern of , which we refer to as confabula- Accepted 11 March 2008 tory hypermnesia, cannot be traced back to any more basic and specific cognitive deficit and Action editor Michael Kopelman is not associated with any particularly unusual pattern of brain damage. Making reference Published online 5 June 2008 to the Memory, Consciousness and Temporality Theory – MCTT (Dalla Barba, 2002), we pro- pose that LM shows an expanded Temporal Consciousness – TC, which overflows the limits Keywords: of time (‘‘Do you remember what you did on March 13, 1985?’’) and of details (‘‘Do you re- Confabulation member what you were wearing on the first day of summer in 1979?’’) that are usually re- spected in normal subjects and in confabulating patients. ª 2008 Elsevier Srl. All rights reserved. Temporal consciousness

1. Introduction Mercer et al., 1977; Schnider et al., 1996a, 1996b; Talland, 1961; Wyke and Warrington, 1960). But confabulation is also Confabulation is a symptom observable in some patients with seen in patients suffering from ruptured aneurisms of the an- memory impairment. At a general level, confabulation can be terior communicating artery, subarachnoid haemorrhage or referred to as a symptom observable in amnesic patients who encephalitis (Alexander and Freedman, 1984; Dalla Barba are unaware of their memory deficit, and which consists of ac- et al., 1997a, 1997b; Delbecq-Derouesne´ et al., 1990; Irle et al., tions and verbal statements that are unintentionally incon- 1992; Kapur and Coughlan, 1980; Kopelman et al., 1995; Luria, gruous to the patient’s history, background, present and 1976; Moscovitch, 1989, 1995; Papagno and Muggia, 1996; future situation (Dalla Barba, 1993a). Schnider et al., 1996a, 1996b; Stuss et al., 1978), head injury This rather infrequent disorder is classically described in (Baddeley and Wilson, 1986; Dalla Barba, 1993b; Schnider Korsakoff’s syndrome (Benson et al., 1996; Bonhoeffer, 1904; et al., 1996a, 1996b; Weinstein and Lyerly, 1968), Binswanger’s Cermak et al., 1980; Dalla Barba et al., 1990; Korsakoff, 1889; (Dalla Barba, 1993a), Alzheimer’s disease and

* Corresponding author. INSERM U. 610, 47 boulevard de l’Hoˆpital, Paris F-75013, France. E-mail address: [email protected] (G. Dalla Barba). 0010-9452/$ – see front matter ª 2008 Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2008.03.009 cortex 45 (2009) 566–574 567

frontotemporal dementia (Dalla Barba et al., 1999; Kern et al., disrupted in a confabulatory patient, and in non-confabu- 1992; Nedjam et al., 2000, 2004) and aphasia (Sandson et al., lating patients with damage. The latter find- 1986). Confabulation may also be observed, on occasion, in ings lead Johnson and colleagues to propose that a reality normal subjects (Burgess and Shallice, 1996; Dalla Barba monitoring, or source monitoring, deficit may occur with et al., 2002; Kopelman, 1987). confabulation but is not the only factor involved in the Within confabulatory behaviour some distinctions have genesis of confabulation (Johnson, 1997). been proposed. Berlyne (1972), following Bonhoeffer (1904), (2) Moscovitch (1989, 1995), Moscovitch and Melo (1997) and distinguished between ‘‘momentary’’ and ‘‘fantastic’’ confab- Gilboa et al. (2006) have proposed that confabulation is ulation. According to Berlyne (1972), momentary confabula- the result of a deficit of strategic retrieval. They propose tion, which invariably must be provoked, is autobiographical a distinction between two components of retrieval. One, in content, refers to the recent past and consists of true mem- associative retrieval, is relatively automatic and indepen- ories displaced in their time context. In contrast, fantastic dent from frontal functions. The other, strategic retrieval, confabulation is spontaneous and ‘‘it is autobiographical, is self-initiated, goal-directed, effortful and intelligent. but entirely invented. The principal content is invariably gran- Within strategic retrieval processes, two further compo- diose and seems to be related to wish fulfilment and prestige nents are hypothesised. The first involves organising seeking’’ (Berlyne, 1972, p. 33). Subsequently Kopelman (1987) a memory search that uses whatever knowledge is avail- argued that Berlyne’s description was inadequate because it able, whether semantic or episodic. Once knowledge is re- failed to isolate the distinguishing features of the two types covered, a second strategic process is involved in of confabulation and proposed to focus on the modality of ap- monitoring the output of the memory search and checking pearance by referring to ‘‘provoked’’ and ‘‘spontaneous’’ con- whether it is consistent with other information in seman- fabulation. Provoked confabulation would reflect a normal tic and episodic memory. When strategic retrieval is dis- response to a faulty memory, whereas spontaneous confabu- rupted, following damage in the ventromedial and lation would reflect the production of an ‘‘incoherent and con- orbitofrontal cortex (Gilboa et al., 2006; Moscovitch, 1982), text-free retrieval of and associations’’ (Kopelman, both semantic and episodic should occur 1987, p. 1482) resulting from the superimposition of frontal if the demands on the strategic retrieval of episodic versus dysfunction on an organic . Schnider et al. (1996a, semantic information are matched. Burgess and Shallice’s 1996b) have suggested that the term ‘‘spontaneous confabula- (1996) model is consistent with Moscovitch’s proposal that tor’’ should only be attributed to patients who show the ten- confabulation is associated with deficits in strategic re- dency to act on their confabulations, since, they argue, trieval, which implicate defective search and monitoring. action is the only observable symptom that cannot be directly provoked by the researcher or some other external trigger. These hypotheses that emphasise the role of a frontal/ However, the distinction between spontaneous and provoked executive dysfunction and of the disruption of monitoring confabulation has not gone unchallenged. In fact it has been processes in the origin of confabulation are challenged by shown that spontaneous confabulations are not necessarily several types of observations: (a) two patients have been ‘‘fantastic and grandiose’’ (Dalla Barba, 1993a; Dalla Barba described with a confabulatory syndrome where there were et al., 1997a, 1997b) and that provoked confabulations can be spared executive functions and no frontal pathology (Dalla fantastic and incoherent (Dalla Barba, 1993b; Dalla Barba Barba, 1993a; Dalla Barba et al., 1990); (b) the confabulating pa- et al., 1998). Accordingly, the line drawn between spontaneous tient described by Delbecq-Derouesne´ et al. (1990) had a docu- and provoked confabulations often appears to be quite an ar- mented frontal lobe lesion but performed normally on tasks bitrary decision. Some authors, in fact, argue that it is not supposed to be sensitive to frontal lesion; (c) the confabulating meaningful to impose a dichotomy, and that confabulation patient described by Dalla Barba et al. (1997a, 1997b) showed should be regarded as a continuous variable, ranging from mi- impaired executive functions without any evidence of struc- nor distortions to the more fantastical (Dalla Barba, 1993b; tural or functional damage to the frontal lobe; (d) in some Fischer et al., 1995; Kapur and Coughlan, 1980). patients confabulation affects the performance on episodic As far as the mechanisms of confabulation are concerned, memory tasks but not on semantic memory tasks (Dalla three major approaches have been proposed. Barba, 1993a; Dalla Barba et al., 1997a, 1997b, 1990), even when demands on the strategic retrieval of episodic versus (1) Johnson argued that confabulation reflects poor source semantic information are matched (Dalla Barba et al., 1997a, monitoring,orreality monitoring, i.e., deciding whether 1997b, 1999). It is also well known that only a relatively small a memory is a trace of something that actually happened proportion of patients with ventromedial and orbitofrontal to you or is a memory of an imagined event (Johnson, lesions confabulate. Retrieval models of confabulation pro- 1991). Damage to frontal/executive functions would result pose that it is a very specific set of cognitive functions that in an impairment of judgment processes involved in real- are not measured by traditional frontal/executive tests that ity monitoring and so in confabulation. This interpretation is disrupted in confabulation. However, these models don’t of confabulation is consistent with the idea that confabu- predict what would be a good measure of the set of frontal/ex- lation is a form of (Moscovitch, 1989; ecutive functions supposed to be involved in strategic re- Schacter et al., 1984) combined with misattribution of tem- trieval and monitoring. poral and spatial context (Schacter, 1987). However, in a more recent paper, Johnson et al. (1997) demonstrated (3) The third approach concerning the mechanisms involved that reality monitoring, or source monitoring, was equally in confabulation predicts that confabulations are the 568 cortex 45 (2009) 566–574

result of a disrupted personal temporality (Dalla Barba, impaired on some tests considered sensitive to executive dys- 1997a, 1997b, 1999, 2000, 2001, 2002). Based on clinical function. He performed pathologically on the Trail Making and experimental, evidence, this hypothesis assumes Test (Davies, 1968) [Trail Marking Test part A 120 sec, 25/25, that in confabulating patients the knowledge of time is <10 percentile; Trail Marking Test part B 4 min, 17/25, <10 per- preserved, in that they are aware of a past, present and fu- centile] and on the Digit Symbol subtest of the Wechsler Adult ture. However, they are unable to distinguish between per- Intelligence Scale Revised (Wechsler, 1981) raw score ¼ 17. His sonal habits, repeated events and routines and true performance on Letter Fluency and on Category Fluency was episodic memories or true personal plans. In spite of also defective, producing an average of 6 and 12 words, re- some important differences, this theory is not incompati- spectively. In contrast, he performed normally on both direct ble with the theory proposed by Schnider and co-workers, (7) and reverse (4) digit span. which posits that confabulators fail to suppress inappro- priate memory traces, resulting in all active traces appear- 2.2.1. Clinical tests of memory ing to relate to the present (but see Dalla Barba, 2000, 2001, On the Free and Cued Selective Reminding Test (Buschke, 2002 for a critique of the concept of memory trace). 1984; see Table 1) LM showed a massive deficit in free , whereas cued recall and recognition were relatively better This paper describes the study of a patient, LM, with a Kor- preserved. On the Logical Memory subtest of the Wechsler sakoff’s syndrome who developed an extraordinary form of Memory Scale – III (Wechsler, 1997; see Table 1), he showed confabulatory syndrome, which we refer to as confabulatory very poor and impaired recognition. In addition, hypermnesia, i.e., the tendency to provide a confabulatory an- his performance on this test was contaminated by many con- swer to questions for which the predicted and most frequently fabulations. The patient also had great difficulty in retrieving observed response in normal subjects and in confabulators is autobiographical episodes and showed very poor knowledge ‘‘I don’t know’’. of famous facts and famous people. The aims of this study are to elucidate as fully as possible the nature of the impairment of patient LM by trying to find 2.3. Examination of confabulation answers to the following questions: ‘‘Can LM’s confabulatory hypermnesia be traced back to LM produced most of his confabulations in informal conversa- a specific cognitive deficit?’’ tion, when answering specific questions and spontaneously, ‘‘What distinguish LM from other confabulating patients mainly referring to autobiographical episodic memory. Con- who do not confabulate answering questions for which the fabulation was always plausible and semantically appropriate expected answer is ‘I don’t know’?’’ so that an hypothetical observer not familiar with LM’s his- tory, background and present situation could hardly tell whether LM’s reports were confabulatory or not. For example 2. Case report he would claim that on the previous day he had a soup for din- ner and then he watched the news on television. In such 2.1. History a case it would be impossible to tell whether this was a confab- ulatory report unless one knew that he didn’t have soup for LM, retired warehouseman of an airways company, is a 68- dinner and that he didn’t watch television because there year-old right-handed man with 8 years of education. He is was no television in the ward where he was hospitalised. married and has five children. He has a history of heavy drinking which lasted more than 2.4. Confabulation Battery 30 years and was stopped approximately 3 months before the present evaluation. To further examine LM’s confabulation, we submitted him to Following the abrupt onset of temporo-spatial disorienta- a new version of the Confabulation Battery (Dalla Barba, tion and memory loss, LM was referred to the Memory Clinic 1993a). The Confabulation Battery involves the retrieval of of the Charles Foix hospital in Ivry-sur-Seine for neuropsycho- various kinds of information and consists of 165 questions, logical evaluation. The physical, neurological and psychiatric 15 for each of the following domains: examination was normal. An MRI brain-scan showed a mild diffuse cortical atrophy without evidence of any focal lesion. The patient’s history of heavy drinking and the clinical picture Table 1 – Memory test results suggested a diagnosis of Korsakoff’s syndrome. LM NCs’ means 2.2. Neuropsychological examination (standard deviation, SD) The patient’s collaboration during the testing sessions was Free and Cued Immediate cued recall 13/16 15.2 (1.4) good. On direct questioning he was disoriented and confabu- Selective Total free recall 6/48 28.9 (6.8) lated in time and space. He scored 15/30 on the Mini Mental Reminding Test Recognition 13/16 15.7 (.5) State Examination (Folstein et al., 1975). On tests of oral ex- pression, understanding of oral language, neglect, ideational, Logical Memory Immediate recall 11/75 Delayed recall 6/50 ideomotor and constructional apraxia, and short-term mem- Recognition 16/30 ory the patient was judged to be normal. LM showed to be cortex 45 (2009) 566–574 569

(1) Personal Semantic Memory (age, date of birth, current ad- Since there is no sufficiently acceptable external criterion ca- dress, number of children, etc.). pable of defining confabulation, for its detection an arbitrary (2) Episodic Memory. Episodic, autobiographical questions. decision necessarily had to be made. In order to distinguish (3) Orientation in Time and Place. between a wrong response and a confabulation a clear-cut de- (4) Linguistic Semantic Memory. Items 16–30 of the Wechsler cision was adopted only for answers to questions probing ori- Adult Intelligence Scale vocabulary subtest were selected entation in time. In this case the most strict criterion was for a word definition task. chosen: answers to questions regarding the current year, sea- (5) Recent General Semantic Memory. Knowledge of facts son, month, day of the month, day of the week and hour of the and people, which have been repeatedly reported in the day were judged to be confabulations only if erring for more news during the last 10 years. For example, ‘‘Who is Ben than 5 years, 1 season, 2 months, 10 days, 3 days or 4 h, respec- Laden?’’ tively. Answers to the other questions of the Confabulation (6) Contemporary General Semantic Memory. Knowledge of Battery were independently rated as ‘correct’, ‘wrong’, and famous facts and famous people from 1940 to 1990. For ‘confabulation’ by four different raters, and interrater reliabil- example, ‘‘What happened in Paris in May 1968?’’ ity was 100%. It must be emphasised that the decision as to (7) Historical General Semantic Memory. Knowledge of fa- whether an answer was wrong or confabulatory was never mous facts and famous people before 1900. For example, puzzling, although it may have been made on an arbitrary or ‘‘What happened in 1789?’’ subjective basis. As far as questions concerning personal (8) Semantic Plans. Knowledge of issues and events likely to and semantic plans are concerned, it might be argued that happen in the next 10 years. For example, ‘‘Can you tell any possible answer is a confabulation, since, by definition, me what you think will be the most important medical the future is only ‘‘probable’’ and there is in principle no ‘‘cor- breakthrough likely to take place in the next 10 years?’’ rect’’ answer to questions about the future. Yet, answers con- (9) Episodic Plans. Personal events likely to happen in the fu- cerning the future can be definitely confabulatory when they ture. For example, ‘‘What are you going to do tomorrow?’’ show a marked discrepancy or a real contradiction with (10) ‘‘I don’t know’’ Semantic. These were questions tapping what a predicted future event might be, in view of the present semantic knowledge and constructed so as to receive situation. For example, although he was hospitalised and de- the response ‘‘I don’t know’’ from normal subjects. For spite the fact that there wasn’t any television in the ward, to example, ‘‘What did Marilyn Monroe’s father do?’’ the question ‘‘What are you going to do to night?’’, LM an- (11) ‘‘I don’t know’’ Episodic. These questions tapped episodic swered ‘‘I’ll have dinner with my wife and then watch the memory and were constructed so as to receive the re- news at the television’’. sponse ‘‘I don’t know’’ by normal subjects. For example, ‘‘Do you remember what you did on March 13, 1985?’’ 3. Results

2.4.1. Procedure LM’s and NCs’ performance on the Confabulation Battery is Questions from the 11 domains were randomised and pre- reported in Table 2. sented to the patient and to 10 age and education matched normal controls (NCs). Responses were scored as ‘correct’’, 3.1. Correct responses ‘‘wrong’’, ‘‘I don’t know’’, and ‘‘confabulation. For episodic memory, responses were scored ‘‘correct’’ when they LM produced significantly fewer correct responses than NC to matched information obtained from the patient’s relatives. questions probing Personal Semantic Memory, Episodic Mem- Correct responses were self-evident for semantic memory ory, Orientation in Time and Place, Recent Seneral Semantic questions. For ‘‘I don’t know’’ questions, both Semantic and Memory [t(9) ¼ 15, p < .001; estimated percentage of normal Episodic, an ‘‘I don’t know’’ response was scored as correct. subjects falling below LM’s scores ¼ .0%], Contemporary

Table 2 – LM’s and NCs’ performance (%) on the confabulation battery Correct Confabulation Wrong IDK Total recall

LM NC LM NC LM NC LM NC LM NC

Personal Semantic Memory 73 100 20 0 0 0 7 0 93 100 Episodic Memory 33 100 53 0 7 0 7 0 93 100 Orientation in Time and Place 53 100 13 0 33 0 0 0 100 100 Linguistic Semantic Memory 66 81.4 (15.7) 0 0 33 9.9 (9.9) 0 8.7 (7.3) 100 91.3 (5.6) Recent General Semantic Memory 33 96.5 (3.7) 40 .7 (2.2) 27 .7 (2.2) 0 2.1 (3.4) 100 97.9 (3.3) Contemporary General Semantic Memory 73 93.2 (7.7) 7 0 13 1.3 (4.1) 7 5.5 (6.2) 93 94.5 (6.1) Historical General Semantic Memory 53 73.2 (28.9) 13 .7 (2.2) 20 13.3 (27) 13 13.2 (10.3) 86 86.8 (4.5) Semantic Plans 80 95.9 (6.5) 7 0 0 1.4 (3) 13 2 (6.3) 87 97.3 (6.4) Episodic Plans 33 98 (6.3) 33 0 27 0 7 2 (6.3) 93 98 (6.3) ‘‘I don’t know’’ Semantic 66 99.3 (2.2) 33 .7 (2.2) 0 0 66 99.3 (2.2) 33 0 ‘‘I don’t know’’ Episodic 7 100 93 0 0 0 7 100 93 0 570 cortex 45 (2009) 566–574

General Semantic Memory [t(9) ¼ 2.3, p < .05; estimated per- probing Personal Semantic Memory, Orientation in Time and centage of normal subjects falling below LM’s scores ¼ 2%], Place, Contemporary General Semantic Memory, Historical Semantic Plans [t(9) ¼ 2.5, p < .05; estimated percentage of nor- General Semantic Memory and Semantic Plans (Chi-square mal subjects falling below LM’s scores ¼ 1.5%], Episodic Plans test, all p < .05). [t(9) ¼ 10.3, p < .001; estimated percentage of normal subjects To summarise, LM produced an impressive percentage of falling below LM’s scores ¼ .0%], and to ‘‘I don’t know’’ Seman- confabulations in response to ‘‘I don’t know’’ Episodic ques- tic [t(9) ¼ 14.4, p < .001; estimated percentage of normal sub- tions. He also produced more confabulations to questions in- jects falling below LM’s scores ¼ .0%], and ‘‘I don’t know’’ volving episodic recall and episodic plans compared to Episodic questions (Crawford and Garrthwaite, 2002; Crawford questions involving recall from semantic memory. and Howell, 1998). LM produced fewer correct responses than NC to questions probing Linguistic Semantic Memory and His- 3.3. Examples of LM’s confabulation for each domain torical Semantic Memory, but this effect was not significant. The estimated percentage of normal subjects falling below 3.3.1. Personal Semantic Memory LM’s scores was 19.7% for Linguistic Semantic Memory and Q. ‘‘What is your brother’s job? 27.3% for Historical Semantic Memory. A. ‘‘Re´my is an artist. He works in variety shows.’’ LM con- LM produced significantly fewer correct responses, i.e., ‘‘I fuses his brother with his son (Patrik) who actually works as don’t know’’, to ‘‘I don’t know’’ Episodic questions than to an artist in variety shows. any other type of question (all p < .0001; estimated percentage of normal subjects exhibiting a difference more extreme than 3.3.2. Episodic Memory LM ¼ .0, Crawford and Garrthwaite, 2002; Crawford and Q. ‘‘Do you remember the last time a doctor examined you?’’ Howell, 1998). Episodic Memory, Recent General Semantic A. ‘‘Well, he examined me without really examining me, Memory and Episodic Plans were also significantly affected because my doctor lives near me, so I see him quite often. compared to Orientation in Time and Place and Historical The last time. not so long ago in any case.’’ General Semantic Memory (all p < .0001; estimated percentage of normal subjects exhibiting a difference more extreme than 3.3.3. Orientation in Time and Place LM ¼ .0), which in turn were impaired compared to Personal Q. ‘‘What month is it?’’ Semantic Memory, Linguistic Semantic Memory, Contempo- A. ‘‘End of December.’’ In fact it was the end of April. rary General Semantic Memory, Semantic Plans, and ‘‘I don’t know’’ Semantic questions (all p < .0001; estimated percent- 3.3.4. Recent General Semantic Memory age of normal subjects exhibiting a difference more extreme Q. ‘‘What does the Mir station remind you of?’’ than LM ¼ .0, Crawford and Garrthwaite, 2002; Crawford and A. ‘‘It’s a metro’s station in the 15th arrondissement in Howell, 1998). Paris.’’ NC produced significantly fewer correct responses to ques- tions probing Linguistic Semantic Memory and Historical Gen- 3.3.5. Contemporary General Semantic Memory eral Semantic Memory than to any other type of question (all Q. ‘‘What happened in May 1968?’’ p < .05) except for questions probing Contemporary General A. ‘‘It was the beginning of the workmen’s revolution; the Semantic Memory. government opposed Africa.’’ To summarise, compared to NC, LM performed poorly across the board on the Confabulation Battery, with his per- 3.3.6. Historical General Semantic Memory formance being relatively better preserved in Personal Seman- Q. ‘‘What does the Dreyfus affaire remind you of?’’ tic Memory, Linguistic Semantic Memory, Contemporary A. ‘‘It’s the story of a poisoning and of a murder.’’ Semantic Memory and Semantic Plans. He was particularly impaired in answering ‘‘I don’t know’’ Episodic questions 3.3.7. Semantic Plans where he correctly answered ‘‘I don’t know’’ only 1 out of 15 Q. ‘‘What do you think will be the most important advance- times. ments in the exploration of space in the next 10 years?’’ A. ‘‘We will land on the Moon and see if somebody lived 3.2. Confabulations there, if it is habitable.’’

NC produced virtually no confabulations. In fact, only one 3.3.8. Episodic Plans subject produced one confabulation in Recent General Seman- Q. ‘‘What are you going to do the day after tomorrow?’’ tic Memory and one in Historical General Semantic Memory. A. ‘‘I’ll go shopping, as usual, and then watch television.’’ A Chi-square test revealed a global significant effect of the type of questions on LM’s confabulations [c2 (10) ¼ 246,9, 3.3.9. ‘‘I don’t know’’ Semantic p < .001]. LM did not confabulate in response to Linguistic Q. ‘‘Who won the Palme d’Or at the Canne Festival in 1980?’’ Semantic Memory questions. He produced significantly more A. ‘‘Fernandel.’’ confabulations to ‘‘I don’t know’’ Episodic questions than to any other type of question (Chi-square test, all p < .001). He 3.3.10. ‘‘I don’t know’’ Episodic also produced significantly more confabulations to Episodic Q. ‘‘Do you remember what you had for dinner on Tuesday Memory, Recent General Semantic Memory, Episodic Plans two weeks ago?’’ and ‘‘I don’t know’’ Semantic questions than to questions R. ‘‘Steak with French fries.’’ cortex 45 (2009) 566–574 571

Q. ‘‘Do you remember what you were wearing on the first subjects and which produce confabulations, but less florid day of summer in 1979?’’ than LM’s, in other confabulating patients (Dalla Barba, R. ‘‘A short and a T-shirt.’’ 1993a; Dalla Barba et al., 1998). Q. ‘‘Do you remember what you did on March 13, 1985?’’ As far as total recall is concerned, i.e., the sum of correct re- A. ‘‘We spent the day at the Senart Forest’’ (a place where sponses, errors and confabulations, LM and NC showed a sim- LM used to go often with his family). ilar pattern of performance. They both showed the tendency Q. ‘‘Do you remember what you did for your 27th to provide an answer, correct or not, rather than an ‘‘I don’t birthday?’’ know’’ response to all types of questions with the exception R. ‘‘Wait a minute. I came back from the army when I was of ‘‘I don’t know’’ questions where LM was always productive, 23, so the 27th birthday. I think. Yes! I had dinner at my fu- whereas NC always correctly answered ‘‘I don’t know’’. ture wife’s place.’’ From LM’s performance on the Confabulation Battery emerges a previously unreported phenomenon, which we re- fer to as confabulatory hypermnesia, i.e., the tendency to provide 4. Discussion a confabulatory answer to questions for which the predicted and most frequently observed response in normal subjects The patient we have described suffers from a relatively pure and in confabulators is ‘‘I don’t know’’. It might be argued amnesic syndrome, in the sense that the memory impairment that LM’s specific pattern of performance reflects a methodo- is not associated with other cognitive impairments likely to logical bias, in that ‘‘I don’t know’’ Semantic questions may be interfere with memory performance. Although he performs more difficult or less likely to elicit confabulations than ‘‘I poorly on the Mini Mental State Examination, mainly due to don’t know’’ Episodic questions. Confabulations in response his disorientation, LM doesn’t show a general deterioration to ‘‘I don’t know’’ questions, both semantic and episodic, of intellectual and attentional abilities, and he scores nor- have been reported in some confabulating patients (Dalla mally on tests of short-term memory. His amnesia involves Barba, 1993b; Dalla Barba et al., 1998; Fotopoulou et al., 2004, memory for both personal and public events, as well as learn- 2007; Kopelman et al., 1997), whereas other patients do not ing of new information as shown in his poor performance on confabulate at all to these questions (Box et al., 1999; Dalla the Free and Cued Selective Reminding Test and on the Logical Barba, 1993a; Dalla Barba et al., 1997a, 1997b). However, Memory subtest of the Wechsler Memory Scale. LM confabu- none of the reported cases confabulated as much as LM to ‘‘I lates both spontaneously and on direct questioning. His con- don’t know’’ Episodic questions, and in none of these cases fabulations are always plausible and never show the bizarre, was there such a clear dissociation between confabulations ‘‘fantastic’’ (Baddeley and Wilson, 1986) or semantically to ‘‘I don’t know’’ Episodic and ‘‘I don’t know’’ Semantic ques- anomalous (Dalla Barba, 1993b) content described in some tions. Actually some patients confabulated slightly more to ‘‘I confabulating patients. don’t know’’ Semantic than to ‘‘I don’t know’’ Episodic ques- On the Confabulation Battery, LM produced fewer correct tions (Fotopoulou et al., 2007). So, although some patients con- responses than NCs to all types of questions, although he per- fabulate to ‘‘I don’t know’’ Episodic questions, none of them formed relatively better in Personal Semantic Memory, Lin- show the specific pattern of performance described in LM. guistic Semantic Memory, Contemporary Semantic Memory This pattern of performance, that we call confabulatory hy- and Semantic Plans than in other domains. This result is sim- permnesia, doesn’t seem to simply reflect differences in task ilar to the pattern of performance of other amnesic patients difficulty. This leads us to address the problem of the origin on the Confabulation Battery (Dalla Barba, 1993b; Dalla Barba of confabulatory hypermnesia. By asking the following ques- et al., 1997a, 1997b; Fotopoulou et al., 2004). In LM, like in other tions: ‘‘Why does LM confabulate when answering episodic patients, semantic memory and semantic plans are better pre- memory questions for which the expected answer is ‘I don’t served than episodic memory and episodic plans. However, know’?’’ and ‘‘What is the difference between LM and confab- unlike other confabulators, LM produced only one correct –‘‘I ulating patients who do not confabulate so floridly with ‘‘I don’t know’’, response to ‘‘I don’t know’’ Episodic questions. don’t know questions’’? To this type of question, 14 out of 15 times he produced It has been argued that confabulation reflects poor source a confabulation. monitoring. Source monitoring refers to the set of processes LM confabulated in response to all types of questions, with involved in making a decision about the origin of different in- the exception of Linguistic Semantic Memory. However, he formation (see Metcalf et al., 2007, for a review). A related con- produced significantly more confabulations in Episodic Mem- cept is reality monitoring, which refers to the ability to ory, Recent Semantic Memory and Episodic Plans compared to discriminate between internally and externally generated in- the other types of questions. Like in other confabulators (Dalla formation (e.g., imagination vs veridical perception). Accord- Barba, 1993a, 1993b; Dalla Barba et al., 1997a, 1997b), LM ing to this view, confabulation is the result of mistaking showed confabulations with a pattern of selectivity, affecting imagined events for truly experienced events (Johnson, the episodic domain more than the semantic domain. He also 1991). This kind of explanation, however, does not account confabulated in Recent General Semantic Memory, which may for the fact that confabulation, as in the present case and in represent a grey area between semantic and episodic memory other studies (Dalla Barba, 1993a, 1993b; Dalla Barba et al., (Shallice, 1988), and in ‘‘I don’t know’’ Semantic questions. But 1990, 1997a, 1997b; Delbecq-Derouesne´ et al., 1990), is absent the most striking aspect of LM’s confabulations is his ten- or significantly less frequent in tasks that require retrieval of dency to confabulate 3 times as much with episodic memory non-episodic information. In fact, if a disruption of reality questions that are usually answered ‘‘I don’t know’’ by normal monitoring were responsible for confabulation, confusion 572 cortex 45 (2009) 566–574

between truly experienced and imagined events and informa- tion should not be limited to episodic retrieval but should ex- tend across all memory domains. Moreover, if we consider the examples of LM’s confabulations in ‘‘I don’t know’’ Episodic questions, there is no evidence that he is mistaking imagined events for really experienced events. Most of his confabula- tions to ‘I don’t know’’ Episodic questions reflect the retrieval of personal habits or semantic information rather than re- trieval of imagined events: the Senart Forest is a place where he used to go often with his family, steak and French fries are a very common meal in France, in summer many people wear shorts and T-shirts. The retrieval of personal habits and semantic information Fig. 1 – A hypothesis concerning the relation between [ in LM’s confabulations could be traced back to a deficit of stra- memory, consciousness and temporality. NS nervous [ tegic retrieval (Moscovitch, 1989, 1995; Moscovitch and Melo, system; X and Y patterns of organisation and activation [ 1997). In the presence of such a deficit, only associative re- of the nervous system; TC temporal consciousness; [ [ trieval is possible and this might be reflected by the type of KC knowing consciousness; U uniqueness; and [ confabulations produced by LM. A deficit of strategic retrieval M multiplicity. applies equally across all domains of memory. In other words, confabulation should equally affect episodic and semantic memory if both episodic and semantic memory tasks require knowing consciousness – KC and temporal consciousness – TC. (2) the involvement of strategic retrieval processes. However, this KC describes the mode of addressing the object in order to hypothesis has difficulties in accounting for cases in which know it. (3) TC describes the mode of consciousness that tem- confabulations are confined to the domain of episodic mem- poralises its object according to the subordinate structures of ory (Dalla Barba, 1993b; Dalla Barba et al., 1990, 1997a, temporality, the past, the present and the future. (4) Con- 1997b), also when both episodic and semantic memory tasks sciousness must necessarily always be consciousness of require the involvement of strategic retrieval processes (Dalla ‘‘something’’. Every type of consciousness is consciousness Barba et al., 1997a, 1997b, 1999). As far as LM’s case is con- of an object. The object of consciousness represents a determi- cerned, a strategic retrieval deficit account predicts that if ‘‘I nation and a indetermination, a Uniqueness and a Multiplicity. don’t know’’ Semantic and ‘‘I don’t know’’ Episodic questions Let’s consider this point closer. This pen on the desk is both make equal demands on strategic retrieval processes then apenand the pen. In the first case it is an undetermined pen, confabulations should occur both for ‘‘I don’t know’’ Semantic something that belongs to the category of ‘‘pens’’, an object and ‘‘I don’t know’’ Episodic questions, which is not what was that I recognize and use appropriately because I recognize it. actually observed. As discussed above, there is no reason to On the contrary, in the second case ‘‘the pen’’ is a determined consider one type of ‘‘I don’t know’’ question more difficult object, is exactly this pen in front of me, the pen I bought yes- or more likely to elicit confabulation than the other type. Since terday and that I will be using tomorrow. So, the pen reveals there is no specific available measure of the amount of strate- a uniqueness and a multiplicity, the multiplicity of being gic retrieval involved in a task, it is impossible to know a pen and not a different object of the object in front of me, whether ‘‘I don’t know’’ Episodic questions are more demand- the uniqueness of being precisely this pen and not another pen. ing in terms of strategic retrieval processes than ‘‘I don’t Within the framework of the MCTT, we have proposed that know’’ Semantic questions. However, there is clear evidence confabulation in episodic memory and in personal future plan- that LM was engaged in an active search when answering ning tasks, as in LM’s case and in other patients (Dalla Barba both ‘‘I don’t know’’ Episodic questions (see his answer to et al., 1997a, 1997b, 1999),canbe interpretedas theresult of a con- the question ‘‘Do you remember what you did for your 27th dition in which TC remains but, in order to remember the per- birthday?’’) and ‘‘I don’t know’’ Semantic questions, as clearly sonal past and plan the personal future, addresses Multiplicity emerges from the following example: as Uniqueness. This condition is schematised in Fig. 2.Inother Q. ‘‘What is the first name of Jimmy Carter’s wife?’’ R. ‘‘Her first name?.(search); no; no though I should know it because she is well known’’; To this type of questions, normal subjects don’t even attempt to search and immediately produce an ‘‘I don’t know’’ response, even when they are explicitly asked to make a plausible guess. We have argued (Dalla Barba, 2000, 2001; Dalla Barba et al., 1997a, 1997b, 1999) that confabulation can be interpreted within the framework of the MCTT (Dalla Barba, 2002), The MCTT, that is schematised in the model presented in Fig. 1, holds that (1) consciousness is not a unitary and generic di- mension that passively receives what comes from outside, but is the set of distinct and original modes for addressing the object. Among the modes of consciousness there is Fig. 2 – Confabulation: TC addresses M as U. cortex 45 (2009) 566–574 573

terms, thisisa condition in which TCisstill working but is no lon- our interpretation best accounts for the LM’s confabulatory ger able to accomplish its usual task, i.e., to distinguish between hypermnesia, other interpretations of this phenomenon can- Multiplicity and Uniqueness in order to set up a personal tempo- not be completely dismissed since a clear double dissociation ral workspace. What TC does instead in this condition is to ad- between ‘‘I don’t know’’ Semantic and Episodic questions has dress Multiplicity of the object as Uniqueness, so that the not been yet reported. Be that as it may, this leaves us with result is that not only unique personal episodes, but also habits a number of open questions: What are the cognitive and neu- or personal semantic information are considered in a personal ral correlates of confabulatory hypermnesia? How are the temporal framework. When asked what they did the previous boundaries of TC normally determined? What is the cause of day or what they are going to do the following day, confabulating their breakdown? What would be the critical test or set of ev- patients of this type typically answer reporting as memories and idence that would confirm or disprove this hypothesis? An- plans what they usually do in their daily life. Although admitted swers to these questions would shed light on confabulatory to the hospital, they will say, for example, that the previous day hypermnesia and on the organisation of TC in general. In theywent outshopping and that thefollowingday will be visiting the absence of further experimental evidence these remain some friends, acts that presumably were part of theirroutine life. unanswered, indeed ‘‘I don’t know’’ questions. This kind of interpretation, however, still doesn’t explain why, unlike other confabulators, LM confabulates to ‘‘I don’t know’’ Episodic questions. The analysis of total recall shows references that, with the exception of ‘‘I don’t know’’ questions, LM and NC have the same performance, a mean of 94% and 95% of re- sponses, respectively. This indicates that both LM and NC have Alexander MP and Freedman M. Amnesia after anterior answers to almost all the questions, although in LM the answer communicating artery aneurysm rupture. Neurology, 34: is often confabulatory, especially in the episodic domain. It also 752–757, 1984. Baddeley A and Wilson B. Amnesia, indicates that, according to the MCTT, in both NC and LM, KC and confabulation. In Rubin DC (Ed), Autobiographical Memory. and TC are working, although the latter is working in an abnor- Cambridge, UK: Cambridge University Press, 1986: 225–252. mal way in LM. However, while in NC, KC and TC respect the Benson DF, Djenderedjian A, Miller BL, Pachana NA, Chang L, boundary of ‘‘I don’t know’’ questions, in LM this boundary is Itty L, et al. Neural basis of confabulation. Neurology, 46: overstepped. What is the nature of this boundary? Why NC 1239–1243, 1996. and most confabulators promptly respond ‘‘I don’t know’’ to Berlyne N. Confabulation. British Journal of Psychiatry,120:31–39,1972. ‘‘I don’t know’’ questions, whereas LM confabulates? Bonhoeffer K. Der korsakowsche symptomenkoplex in seinen beziehungen zu den verschiedenen krankheitsformen. One possibility is that LM may have always been a cognitive Allgemeine Zeitung Psychiatrie, 61: 744–752, 1904. ‘outlier’, in the sense that, even premorbidly, he may have Box O, Laing H, and Kopelman MD. The evolution of spontaneous used unusual cognitive strategies and that his confabulatory confabulation, delusional misidentification and a related hypermnesia is a continuation of the use of such strategies. in a case of severe head injury. Neurocase, 5: 251–262, However, no evidence in this sense emerged from questioning 1999. the patient’s wife. So, although this possibility cannot be ex- Burgess PW and Shallice T. Confabulation and the control of Memory cluded, there is no specific evidence favouring a premorbid recollection. , 4: 359–411, 1996. Buschke H. Cued recall in amnesia. Journal of Clinical personality account of LM’s disorder. Neuropsychology, 6: 433–440, 1984. LM’s confabulatory hypermnesia doesn’t seem to be corre- Cermak LS, Uhly B, and Reale L. specificity in the alcoholic lated to any specific pattern of brain damage. The MRI brain- Korsakoff patient. Brain and Cognition, 11: 119–127, 1980. scan showed a mild diffuse cortical atrophy, which is an Crawford J and Garrthwaite P. Investigation of the single case in unremarkable finding. LM’s cognitive profile was also unre- neuropsychology: confidence limits on the abnormality of test markable. In particular, he didn’t show an especially severe scores and test scores differences. Neuropsychologia, 40: 1196–1208, 2002. impairment of executive functions, compared to other con- Crawford J and Howell D. Comparing an individual’s test score fabulators. Accordingly, LM’s confabulatory hypermnesia against norms derived from small samples. The Clinical cannot be traced back to any specific pattern of brain damage Neuropsychologist, 12: 482–486, 1998. or of cognitive impairment. From a merely descriptive point of Dalla Barba G. Confabulation: knowledge and recollective view, and making reference to the MCTT, LM, compared to experience. Cognitive Neuropsychology, 10: 1–20, 1993a. normal subjects and to other confabulators, shows an ex- Dalla Barba G. Different patterns of confabulation. Cortex, 29: panded TC, which overflows the limits of time (‘‘Do you re- 567–581, 1993b. Dalla Barba G. Memory, consciousness and temporality: what is member what you did on March 13, 1985?’’) and of details retrieved and who exactly is controlling the retrieval? In (‘‘Do you remember what you were wearing on the first day Tulving E (Ed), Memory and Consciousness and the Brain: The of summer in 1979?’’) that are usually respected in normal Tallin Conference. Philadelphia: Psychology Press, 2000: 138–155. subjects and in confabulating patients. Dalla Barba G. Beyond the memory trace paradox and the fallacy of the homunculus: a hypothesis concerning the relation between memory, consciousness and temporality. Journal of 5. Conclusions Consciousness Studies, 8: 51–78, 2001. Dalla Barba G. Memory, Consciousness and Temporality. Boston: Kluwer Academic Publishers, 2002. We have described a previously unreported phenomenon, Dalla Barba G, Boisse´ M-F, Bartolomeo P, and Bachoud-Le´vi A-C. confabulatory hypermnesia, arguing that it reflects an expan- Confabulation following rupture of posterior communicating sion of TC beyond its normal limits. Although we believe that artery. Cortex, 33: 563–570, 1997a. 574 cortex 45 (2009) 566–574

Dalla Barba G, Cappelletti YJ, Signorini M, and Denes G. Korsakoff SS. Etude me´dico-psychologique sur une forme des Confabulation: remembering ‘‘another’’ past, planning maladies de la me´moire. Revue Philosophique, 28: 501–530, 1889. ‘‘another’’ future. Neurocase, 3: 425–436, 1997b. Luria AR. The Neuropsychology of Memory. New York: John Wiley, Dalla Barba G, Cipolotti L, and Denes G. Autobiographical memory 1976. loss and confabulation in Korsakoff’s syndrome: a case report. Mercer B, Wapner W, Gardner H, and Benson F. A study of Cortex, 26: 525–534, 1990. confabulation. Archives of Neurology, 34: 429–433, 1977. Dalla Barba G, Mantovan MC, Cappelletti YJ, and Denes G. Metcalf K, Langdon R, and Coltheart M. Models of confabulation: Temporal gradient in confabulation. Cortex, 34: 417–426, a critical review and a new framework. Cognitive 1998. Neuropsychology, 24: 23–47, 2007. Dalla Barba G, Mantovan MC, Traykov L, Rieu D, Laurent A, and Moscovitch M. A neuropsychological approach to memory and Devouche E. The functional locus of intrusions: encoding or perception in normal and pathological aging. In Craik FIM and retrieval? Journal of Clinical and Experimental Neuropsychology, Trehub S (Eds), Aging and Cognitive Processes. New York: 24: 633–641, 2002. Plenum Press, 1982. Dalla Barba G, Nedjam Z, and Dubois B. Confabulation, executive Moscovitch M. Confabulation and the frontal systems: Strategic functions and source memory in Alzheimer’s disease. versus associative retrieval in neuropsychological theories of Cognitive Neuropsychology, 16: 385–398, 1999. memory. In Roedinger HL and Craik FI (Eds), Varieties of Davies A. The influence of age on trial making test performance. Memory and Consciousness: Essay in Honor of . Journal of Clinical Psychology, 24: 96–98, 1968. Hillsdale NJ: Lawrence Erlbaum., 1989: 133–160. Delbecq-Derouesne´ J, Beauvois MF, and Shallice T. Preserved Moscovitch M. Confabulation. In Schacter DL (Ed), Memory recall versus impaired recognition. Brain, 113: 1045–1074, 1990. Distortion. Cambridge: Harvard University Press, 1995: 226–251. Fischer RS, Alexander MP, D’Esposito M, and Otto R. Moscovitch M and Melo B. Strategic retrieval and the frontal Neuropsychological and neuroanatomical correlates of lobes: evidence from confabulation and amnesia. confabulation. Journal of Clinical and Experimental Neuropsychologia, 35: 1017–1034, 1997. Neuropsychology, 17: 20–28, 1995. Nedjam Z, Dalla Barba G, and Pillon B. Confabulation in a patient Folstein MF, Folstein SE, and McHugh PR. ‘‘Mini mental state’’: with frontotemporal dementia and in a patient with a practical method for grading the cognitive state of patients Alzheimer’s disease. Cortex, 36: 561–577, 2000. for the clinician. Journal of Psychiatric Research, 12: 189–198, Nedjam Z, Devouche E, and Dalla Barba G. Confabulation, but not 1975. executive dysfunction discriminate ad from frontotemporal Fotopoulou A, Conway M, and Solms M. Confabulation: motivated dementia. European Journal of Neurology, 11: 728–733, 2004. reality monitoring. Neuropsychologia, 45: 2180–2190, 2007. Papagno C and Muggia S. Confabulation: dissociation between Fotopoulou A, Solms M, and Turbull O. Wishful reality distortions everyday life and neuropsychological performance. Neurocase, in confabulation: a case report. Neuropsychologia, 42: 727–744, 2: 111–118, 1996. 2004. Sandson J, Albert ML, and Alexander M. Confabulation in aphasia. Gilboa A, Alain C, Stuss DT, Melo B, and Moscovitch M. Cortex, 22: 621–626, 1986. Mechanism of spontaneous confabulations: a strategic Schacter DL. Memory, amnesia and frontal lobe dysfunction. retrieval account. Brain, 129: 1319–1414, 2006. Psychology, 17: 21–36, 1987. Irle E, Wowra B, Kunert HJ, and Kunze S. Memory disturbances Schacter DL, Harbluk JL, and McLachlan DR. Retrieval without following anterior communicating artery rupture. Annals of recollection: an experimental analysis of source amnesia. Neurology, 31: 473–480, 1992. Journal of Verbal Learning and Verbal Behavior, 23: 593–611, 1984. Johnson MK. Reality monitoring: evidence from confabulation in Schnider A, Gutbrod K, and Schroth G. Memory without context: organic brain disease patients. In Prigatano GP, and amnesia with confabulations after infarction of the right Schacter DL (Eds), Awareness of Deficit After Brain Injury. New capsular genu. Journal of Neurology, Neurosurgery and Psychiatry, York–Oxford: Oxford University Press, 1991: 176–197. 61: 186–193, 1996a. Johnson MK. Source monitoring and memory distortion. Schnider A, von Da¨niken C, and Gutbrod K. The mechanisms of Philosophical Transactions of The Royal Society of London B Series B: spontaneous and provoked confabulations. Brain, 119: Biological Science, 29: 1733–1745, 1997. 1365–1375, 1996b. Johnson MK, O’Connor M, and Cantor J. Confabulation, memory Shallice T. From Neuropsychology to Mental Structure. Cambridge: deficits, and frontal dysfunction. Brain and Cognition, 34: Cambridge University Press, 1988. 189–206, 1997. Stuss DT, Alexander MP, Lieberman A, and Levine H. An Kapur N and Coughlan AK. Confabulation after frontal lobe extraordinary form of confabulation. Neurology, 28: 1166–1172, dysfunction. Journal of Neurology, Neurosurgery and Psychiatry, 1978. 43: 461–463, 1980. Talland GA. Confabulation in the Wernicke–. Kern R, Van Grop W, Cummings J, Brown W, and Osato S. Journal of Nervous and Mental Disease, 132: 361–381, 1961. Confabulation in Alzheimer’s disease. Brain and Cognition, 19: Wechsler D. Wechsler Adult Intelligence Scale – Revised Manual. New 172–182, 1992. York: Psychological Corporation, 1981. Kopelman MD. Two types of confabulation. Journal of Neurology, Wechsler D. Wechsler Memory Scale – III. New York: Psychological Neurosurgery and Psychiatry, 50: 1482–1487, 1987. Corporation, 1997. Kopelman MD, Guinan EM, and Lewis PDR. Delusional memory, Weinstein E and Lyerly O. Confabulation following brain injury. confabulation, and frontal lobe dysfunction: a case study in de Archives of General Psychiatry, 18: 348–354, 1968. Cle´rambault’s syndrome. Neurocase, 1: 71–77, 1995. Wyke M and Warrington E. An experimental analysis of Kopelman MD, Ng N, and Van Den Brouke O. Confabulation confabulation in a case of Korsakoff’s syndrome using extending across episodic, personal and general semantic a tachistoscopic method. Journal of Neurology, Neurosurgery and memory. Cognitive Neuropsychology, 14: 683–712, 1997. Psychiatry, 23: 327–333, 1960.