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The fractionation of retrograde amnesia
BRAIN
AND
COGNITION
7, 184-200 (1988)
The Fractionation of Retrograde Amnesia ELIZABETH
K. WARRINGTON AND ROSALEEN A. MCCARTHY
National
Hospital,
Queen Square, London
WCIN 3BG
This single case study describes our investigations of the retrograde memory deficit of a patient who became severely and selectively amnesic after an encephalitic illness. On clinical assessment his retrograde deficit for both personal and public events appeared to encompass his entire adult life. However, he retained knowledge of words introduced into the vocabulary during the retrograde period. The experimental investigation documented his inability to recall, recognize, and place in temporal order the names and faces of famous people for all time periods sampled. By contrast, his recall of either a famous face or a famous name was significantly facilitated by the verbal cue of the person’s first name and initial of the surname (i.e., Margaret T . .). His performance on a test of “familiarity” that required him to select the famous name or the famous face from two distracters (unknown) was within normal limits. It is argued that names and faces of famous people are represented in more than one system: both in a vocabulary-like fact memory system that is preserved and also in a cognitively mediated schemata that in this case is functionally inoperative. 0 1988 Academic Press, Inc.
Since Korsakoff’s classical observations, long periods of retrograde amnesia have presented the psychologist and neurologist alike with a conundrum. On the one hand very long periods of retrograde amnesia for events have been reported, stretching in some instances through the individual’s entire life span. At the same time such syndromes can be associated with preserved knowledge of factual information, some of which may have been acquired during the retrograde period. This has given rise to debate as to whether retrograde memories and factual memories are on some continuum only differing in trace strength, or alternatively We thank Dr. G. Stern, Department of Neurology, University College Hospital, London, for referring R.F.R. to this department for psychological assessment. We are also grateful to Dr. P. C. Gautier-Smith for arranging his admission to the National Hospital for further investigations. We thank Chris Brown for her assistance in testing the control subject. Rosaleen McCarthy’s research is supported by the University of Cambridge; her present address is Department of Experimental Psychology, University of Cambridge, Downing Street, Cambridge, CB2 3EB, England. Address reprint requests to Prof. Elizabeth K. Warrington, National Hospital, Queen Square, London, WClN 3BG, England. 184 0278-2626/88$3.OO Copyright All rights
0 1988 by Academic Press, Inc. of reproduction in any form reserved.
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whether they implicate the involvement of two relatively independent subsystems. Those who view memory for facts and memory for events as forming a continuum would argue that the information that amnesics are able to recall is highly overlearned and/or has the status of procedural knowledge. The probability of item recall is therefore postulated to be a function of “trace strength.” To support this notion of a continuum they would cite evidence that in some severe amnesic patients subtle deficits in the processing of factual information can be demonstrated. Thus it is argued that a continuum can be demonstrated between recently acquired information which cannot be retrieved at all, and more distant information for which the deficit is much less obvious (e.g., Cohen & Squire, 1981; Squire, Cohen, & Nadel, 1984).However, impairments in factual knowledge processing are by no means a necessary concomitant of amnesia. Thus both Meudell, Mayes, and Neary (1981), and Warrington and Weiskrantz (1982) reported evidence from a series of R.T. experiments which indicated that amnesics were not significantly different from control subjects in their ability to access category exemplars and antonyms. Indeed such evidence has been interpreted as favoring a discontinuity between memory for facts and memory for events (e.g., Tulving, 1983). More direct evidence for discontinuity may be adduced from patients with profound deficits affecting certain aspects of factual memory, who can in no sense be regarded as having an amnesic syndrome. Warrington (1975) described three patients with progressive degenerative cortical pathology in whom knowledge of both visual and verbal factual information was selectively impaired. At the same time their memory for ongoing events (within the constraints imposed by their loss of factual knowledge) appeared to be satisfactory (Warrington, 1975). One of these patients was formally tested and was shown to score at a near normal level on verbal learning tasks on which amnesic patients failed (Coughlan & Warrington, 1981). We have since investigated two further cases with this syndrome both of whom had profound and widespread impairments such that their verbal vocabulary was reduced to the most rudimentary level. (McCarthy & Warrington, 1986 and 1987). Nevertheless, both patients were employed in full-time jobs which necessitated working without supervision (which is clearly beyond the abilities of patients with a global amnesic syndrome). Since the issue of continuity versus discontinuity hinges upon the properties of retrograde amnesia, the question arises as to how best to specify this deficit (or deficits). Commonly the quantitative investigation of this problem has tested the knowledge of public events and personalities antedating the illness, which has the advantage of providing an objective measure of memory. However, such techniques have proven somewhat problematic, in that baseline “normal” forgetting curves have differed between investigations, thereby resulting in different estimates
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of memory loss in the amnesic patient (see Cermak & Butters, 1986 for a full discussion of this issue). Thus in the original investigation using these methods, negatively accelerated age-related serial position curves were obtained in a large standardization sample, (Warrington & Sanders, 1971), while amnesic patients showed an apparently absolute deficit for all time periods sampled (Sanders & Warrington, 1971). When questions and testing procedures are adjusted so that amnesic patients do not have an absolute deficit, control subjects no longer show the expected forgetting function (Albert, Butters, & Levin, 1979). It is now widely accepted that such techniques are vulnerable to many sources of artifact (Weiskrantz, 1985) and more recent evidence appears to suggest that they may give a misleading and/or incomplete estimate of the amnesic patients’ residual capacities for “remembering” remote events (Cermak & O’Connor, 1983). We have recently had the opportunity to investigate an amnesic patient whose memory for both recent and more distant events was severely impaired. In this report we describe a series of tests designed to manipulate different methods of testing retention for events which spanned his adult life. To this end we investigated his ability to recognize, recall, describe, and identify well-known people, using verbal and visual material. We have been able to document a number of unexpected task-dependent dissociations suggesting that there may be multiple long-term memory representations for this class of information. We will argue that our findings are incompatible with any simplistic continuum model of retrograde memory loss. CASE HISTORY R.F.R. was a 54-year-old (15.3.32) police officer who was admitted to the National Hospital Queen Square on 2.12.86 for further investigations of his severe and persistent memory difficulties. In July 1985 R.F.R. had suffered a pyrexial illness and became extremely confused. This was followed by a lowering in his level of consciousness and he was admitted to the Royal Free Hospital under the care of Dr. Harban where he was observed to be comatose. A lumbar puncture was performed and he had a white cell count of 150 with 95% lymphocytes. A C.T. scan at this stage was normal and his EEG showed mild diffuse abnormalities. He was treated with acyclovir and steroids. His level of consciousness gradually improved but it then became evident that he had a severe anterograde and retrograde amnesia. A repeat C.T. scan (23.1.87) demonstrated asymmetrical areas of low attenuation confined to both temporal lobes with extensive damage in the right temporal region, and in the left temporal lobe the abnormal region was confined to the medial surface (McCarthy & Warrington, in preparation). He was considered to have suffered a herpes simplex encephalitis.
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PSYCHOLOGICAL TEST FINDINGS R.F.R. was originally tested on the WAIS in August 1985 and he obtained a verbal IQ of 117 and a performance IQ of 99. He was reassessed in January 1986 by which time his verbal IQ had improved to 128 and his performance IQ to 110. He obtained a reading IQ equivalent of 120 which is in good accord with his verbal IQ but suggeststhat his performance IQ might be slightly below his optimal level. On specific tests of language function his performance was entirely satisfactory. He had no difficulty whatever in completing a shortened version of the token test of language comprehension. He scored 145/150 correct on the Peabody Picture Vocabulary Test. He scored at an average level on a stringent graded difficulty naming test (McKenna & Warrington, 1980). His explanation of proverbs was satisfactory. His verbal fluency was excellent (a task he approached using very efficient “alphabetic” strategies) for example in 1 min he was able to generate 20 words beginning with the letter “b,” 21 words beginning with the letter “s,” 15 boys names, 16 occupations, and 24 animals. His perceptual and spatial skills appeared to be intact he was able to identify 20/20 incomplete letters and 19/20 unusual view photographs, and scored 18/20 on a same/different face matching test (Warrington, 1982). He also scored within the normal range on tests of spatial discrimination and cube analysis (Whiteley 8z Warrington, 1978). In contrast to his well-preserved intellectual, language, and perceptual abilities he was profoundly and severely amnesic. Thus he was totally unable to maintain any record of ongoing events, he was completely disoriented in time and place, and he was quite unable to give an account of his present circumstances. Not only was there evidence of a marked anterograde memory deficit, but there was also evidence of a severe retrograde deficit stretching into the remote past. On formal memory testing he scored at a chance level on two parallel forms of the verbal and visual recognition memory tests (Warrington, 1984). He scored 31/50 and 27/50 on the verbal versions and 32/50 and 26/50 on the visual versions. On a three-choice recognition memory test for colored photographs of Camden scenes he scored 8/30. On a verbal paired associate learning test his performance was markedly impaired scoring 8/24 and he showed no improvement with a second attempt 6/24. His scores were at a worse level than the poorest control (C. Brown, personal communication). Likewise his story recall (Wechsler Memory Scale) was severely impaired even on immediate recall. On the memory for designs test (WMS) his recall was fragmentary in the extreme. In summary R.F.R. presents with an exceptionally selective and severe amnesia. His cognitive abilities have been shown to be well preserved whereas there is a dense and profound anterograde and retrograde memory
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loss. In this report we focus on his retrograde memory deficit: first reporting a clinical description and second our experimental investigations.
CLINICAL DESCRIPTION OF RFR’s RETROGRADE AMNESIA R.F.R.‘s retrograde amnesia affected both personal and public events stretching into the remote past. Indeed he was unable to give a detailed or coherent account of any episode from either domain. Although he was able to provide a skeleton autobiography it was sparse, having the characteristics of a mere outline lacking in real substance. On questioning he was unable to elaborate on specifc points. He appeared to have little memory for many of the most salient events in a person’s life. For example, he knows that he was stationed in Egypt during his service with the R.A.F. but he commented “I am not sure if I got to Cairo.” Asked about his honeymoon he replied “Europe somewhere, don’t know where.” Given the choice Brussels, Paris, Rome, he said “not Rome I don’t think I have been to Rome, I have an affection for Paris, so it must have been Paris I guess.” He does not appear to realize that his mother died 6 years ago. As for public events he claims he can recall nothing at all. The whole tenor of his conversation is pervaded by uncertainty and repetitiveness and he was to some extent aware of this: for example, in the course of half an hour he might say half a dozen times “I have probably told you a hundred times that I have a very high DRAG rating, I’m sorry I don’t mean to bore you.” He was shown a number of family photographs presented out of context from albums provided by his wife. A number of notable failures occurred. Although he usually recognized photographs of his children he failed to recognize them when they were younger. Even pictures taken 4 or 5 years ago were not always recognized. He hesitantly recognized his mother in several photographs. On one occasion he failed to identify his grandparents. Longstanding friends and colleagues were all strangers to him. Perhaps most telling were his failures to recognize both recent and older photographs of his wife. Structured
Interview
We interviewed both R.F.R. and his wife putting the same questions, spanning the period of their marriage, to each. These questions probed the major salient events of their lives during the last 20 years. R.F.R.‘s responses were very sparse by comparison with his wife’s (see samples in Appendix 1). Autobiographical
Memory
On seven separate occasions R.F.R. was asked to write an account of his life using the following headings: (a) Schooldays, (b) Time in the services, (c) Career with police, (d) Marriage and family. He was en-
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AMNESIA
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couraged to take his time and provide as much detail as he could. The first and final of these accounts are given in full in Appendix 2. His five intervening accounts were substantially identical (down to the level of the specific vocabulary which was used). His descriptions under each heading are very brief indeed and all these skeletal accounts appeared to be retrieved with difficulty. They have many of the characteristics of those memories described as “personal semantics” by Cermak and O’Connor (1983). On no occasion did he recall having previously been asked to write such an account. Probe Word Recall
The Crovitz and Schiffman (1974) technique was used to elicit memories from his past life. Three of his responses to 22 key words suggested that he was recalling a specific rather than a generic event. One of his more precise responses was to the word “tree.” “As a child I was . . . a youth . . . reprimanded by my mother for climbing one of the trees in the back garden . . . . Three trees and the middle one had a branch which came up horizontally, 18 feet above the ground. I used to perch on the tree. I remember having conversations with the boy in the next garden while sitting on this branch.” Public Events
He was asked 20 questions about major events of the last 15 years. He was only able to give an adequate reply to one of these (viz.) who are the boat people). Seven age-matched controls obtained a mean score of 15 (range 1l-20 correct). New Word Vocabulary
His ability to define a “new word” word vocabulary stands in striking contrast to his otherwise dense retrograde amnesia. He was asked to define 50 new words and company names that have come into the (English) vocabulary within the last 20 years. Some examples are as follows: Provisionals-members of the IRA a form of terrorist organization intent on unifying Ireland. AIDS-illness or disease-the aids virus. Thatcherism-word applied to the policies adopted by Margaret Thatcher. Ultraconservatism basically a conservative policy. Shuttle-space shuttle-passenger carrying spaceship-not just a rocket it’s for both landing and re-taking off. Telecom-British telecom organization responsible for communication, telephones telegrams, etc.-Nationalized. His only error in the entire corpus was to define “Telecom” as Nationalized rather than Privatized.
190 EXPERIMENTAL
WARRINGTON
AND
INVESTIGATION
MC CARTHY
OF RETROGRADE
AMNESIA
Experiment 1 In an investigation of retrograde amnesia, comparing naming and recognition of photographs of contemporary personalities with personalities who had faded from view at various time periods in the past, Sanders and Warrington (1971) found that amnesic patients showed marked impairments at all time periods sampled on both versions of the task. Using identical stimuli and procedures R.F.R. was tested on items from the three most recent time periods investigated in that study: namely, 15 contemporary personalities (in the forefront of the news in the late 196Os), 15 personalities who had faded from view by the early 1960s and 15 personalities who had faded from view by the second half of the 1950s). He was first asked to identify each personality and in the event of failure he was given three choices: the target name together with two equally famous distractor names. Contemporary control data was obtained using 10 age-matched male controls (hospital staff). Results The percentage correct for R.F.R. and the mean percentage correct for the control group are given in Table 1. In the control group there was a small decrement in performance related to the remoteness of the famous person. For this stimulus material, on the recognition version of the task, their performance was near to ceiling. In contrast R.F.R. only succeeded in identifying 1 of these 45 personalities and in the recognition version of this task his performance was not significantly different from chance. Comment It is generally accepted that in amnesia due to Wemike-Korsakoff encephalopathy there may be long periods of retrograde amnesia. However, there has been some debate as to the presence of retrograde impairments in amnesia due to medial temporal lobe damage (see Parkin, 1984 for review). R.F.R., like one of the original cases reported by Sanders and Warrington, has damage to the medial surface of the temporal lobes but nevertheless shows evidence of a severe retrograde impairment on this naming and recognition test for faces of famous personalities. EXPERIMENT
2
Cued recall and/or word completion techniques have been shown to have robust facilitatory effects for amnesic patients. In this context it is of some interest to note that those studies claiming that there may be a considerable degree of retrograde memory preservation in some amnesics have tested the recall of retrograde “memory” using cueing techniques
x = 11.5 SD = 2.12
2 SD = 2.98
SD = < I
R. F. R. Controls (N = IO)
Naming photograph with cue
Generating name from auditory cue
R. F. R.
Controls (N = 10) R. F. R. Controls (N = 10)
Naming Photograph
TABLE 2
1 z = 7.75
Recall 7 x = 13.1 SD = I.51
Recognition
Time period early 1960s
7 x = 14.9
Recognition
Late 1960s
SD = 2.68
0 x = 5.25
Recall
x == 8.7 SD 3.6 II x = 14.0 SD = 1.34 I2 2 = 8.7 SD = 3.21
0
Contemporary personality
SD =
x =
SD =
I3 6.8 1.5
2.05
6.8 2.89 9 x = 11.3
x == SD
I
Mid-1970s
Time Period
SD =
x =
SD =
2.92
II 5.5
2.33
6.3 2.68 7 x = 11.4
2 == SD
1
Mid- to late-1960s
SD = < 1
5 x=11.9
Recognition
Late 1950s
CUEING RECALL OF NAMES OF PHOTOGRAPHSOF FAMOUS PEOPLE AND GENERATING THESE NAMES FROM AN AUDITORY CUE
R. F. R. Age-matched controls (N = 8)
Recall
TABLE I RECALL AND RECOGNITION OF FAMOUS FACES
F
E
Ei
F 1’1
2 ZI
R
2 0 crl
2
5 5
2
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but do not systematically differentiate between those memories retrieved in “naming” or “cued” conditions (e.g., Albert et al., 1979). Our aim in this experiment was to attempt to replicate the early observations of a dissociation between “cueing” and “naming” conditions (MarslenWilson & Teuber, 1975; Sanders & Warrington, 1975) in a patient in whom a particularly severe retrograde impairment has been demonstrated. Procedure The stimulusmaterialconsistedof photographsof public figures.Fifteensetsof three personalitieswho hadbeenfamiliarin oneof two time periodsand had since faded from public view (mid-1970s mid-to late-l%Os) together with one contemporary figure were constructed. The three individuals comprising each set were closely matched for occupational status and importance, e.g., David Steele, Jeremey Thorpe, and Jo Grimmond (Liberal party leaders); Len Murray, Vie Feather, and George Woodcock (Trades Union Leaders). R.F.R. was asked to name each personality and when unable to do so he was asked to retrieve the person’s surname when provided with the Christian name and the inital letter of the surname. On a subsequent testing session he was presented with the Christian name and initial letter of each of surnames of each of the 45 personalities and asked to generate/guess the appropriate famous name. For both the pictorial and auditory conditions the 45 photographs were presented in a pseudo-random order with regard to both era and personality “types.” Two independent age-matched control groups were tested; 10 on the visual and 6 on the verbal version of the task.
Results The percentage correct for the naming task and for each of the cuing conditions is given in Table 2. R.F.R. is far worse than the poorest control in the naming task; however, he performed at a level equivalent to the controls in the photograph + cue condition and was better than control subjects when asked to guess or generate any famous name on the basis of the verbal cue alone. Comment These findings replicate the original findings of Sanders and Warrington (1975) in showing a significant facilitatory effect of cuing in naming famous people. Clearly the very robust word completion effects obtained in many investigations of amnesic patients are not necessarily confined to material which is a component of long established linguistic representations (e.g., words acquired in the course of language development). In this experiment we have established that such word completion effects may be at least as powerful for a proper name vocabulary acquired relatively recently (during the last 5 to 15 years), and certainly for a vocabulary learned well within the period for which he has a “retrograde amnesia.” Our two groups of matched control subjects found the photograph + cue version of the task somewhat easier than the “cue alone” condition. We would not wish to claim that there was a reversal of this effect for R.F.R. insofar as he may have benefited from prior exposure in the visual +
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cue condition. Nevertheless we would claim that this pattern of results suggests that the cueing condition was eliciting items from his vocabulary, rather than simply facilitating retrieval from a weak trace. Some implications of these findings will be discussed below. EXPERIMENT
3
In Experiment 2 in which we investigated word completion effects of well-known peoples names with and without a photograph of the individual, there was evidence of considerable implicit knowledge of public figures, but at the same time little evidence of any explicit knowledge insofar as in the naming condition he was very markedly impaired. The question therefore arises as to whether his impairment on such tasks was dependent upon the requirement to verbalize his responses. To this end we explored his ability to place photographs and names of public figures in their appropriate temporal order. Procedure Two groups of five normal subjects were tested on tasks requiring them to pick out the most contemporary and the most remote personality, one group being tested with a face stimulus and the other with a spoken name. On the basis of their performance a subset of 10 items was selected on which the number of items totally correct was relatively high (88% for the visual version and 82% for the auditory version). These items were given to R.F.R. first for ordering of the photographs and second for ordering of the spoken names.
Results This task, which was designed to give a near ceiling effect with normal subjects, was extremely difficult for R.F.R. He was only able to order two of the photographs sets correctly and to order only one of the spoken name sets correctly. This level of performance is no better than that which would be expected by chance. Comment This experiment indicates that R.F.R.‘s retrograde amnesia extends to tasks without an explicit verbal component. These findings, at the very least, provide evidence for a dissociation between names and faces as entries in a vocabulary-like system and names and faces as “temporal” events. This dissociation will be discussed in greater detail below. EXPERIMENT
4
In Experiment 2 using cueing techniques we demonstrated that R.F.R. retained his vocabulary for a number of names of public figures from the recent past. The aim of this experiment was to obtain further evidence of R.F.R.‘s visual and verbal “vocabulary” for famous personalities using a measure of verbal and visual name and face familiarity.
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FIG. I. Examples of face familiarity test stimuli with one famous face and two unknown distractor items.
Method Two sets of 15 names and photographs of famous people were assembled; one set was of personaIities who were prominent in the early 198Os,the other of people who had been most famous approximately 10 to 15 years previously, and who had since faded from prominence. In the verbal version each famous name was paired with two unknown, but “similar” distractor items (e.g., Shirley Williams, Joan Ingham, and Christine Sandys; Ian Paisley, Frank Smith, and Stan Hughes). Correct responses were followed by a request for the individual’s name. In the visual version photographs of unknown people who were somewhat similar in appearance were used (see Fig. I). R.F.R. was asked to indicate which was the famous name or face from arrays or lists of three items (the target and two distractors) in which the target item occurred equally often in each position. The visual version was presented on 1 day, and the auditory version was tested on a subsequent occasion. Eight age-matched controls were tested on the visual version of the task.
FRACTIONATION
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OF RETROGRADE AMNESIA TABLE 3
FACE AND NAME
FAMILIARITY
TEST
Time period 1980-1985 Face naming
R. F. R. Controls (N = 8)
Face selection
R. F. R. Controls (N = 8)
Name selection
R. F. R.
2
x = to.1 SD =
2.93 13 2 = 13.25 SD = 1.47
15
1970-1980 1 8.1 2.6 12 x = 13.75 SD = 1.28 14
? = SD =
Results The percentage correct for R.F.R. on both the visual and the verbal versions of the task and for the matched control group on the visual version is given in Table 3. R.F.R.‘s level of performance was at the lower limits of normal on the visual version and he made only one error on the verbal version. Comment R.F.R.‘s performance on this task is exceptionally good considering his very impaired performance on tasks requiring him to match a photograph of a famous person to one of three equally famous spoken names. Taken together with his performance on the name completion task these findings provide direct evidence that he not only has a famous name vocabulary, but that he also has a famousface vocabulary. He therefore has preserved ability to make familiarity judgments on a class of material which has hitherto provided the archetypal stimulus material for testing retrograde amnesia. Discussion
In this series of experiments we have reported our investigations of a severely amnesic patient whose intellectual and cognitive skills were otherwise entirely satisfactory. In this account we have focused on the retrograde component of his global memory deficit. In our clinical case report we document the pervasive and dense nature of his retrograde amnesia. On the basis of structured interviews and his own written autobiographical accounts his deficit appeared, at the very least, to encompass his entire adult life. Despite this exceptionally severe retrograde deficit, there was evidence that R.F.R. was able to recall a new word vocabulary (e.g., AIDS) which was acquired during the same period. On a questionnaire designed to probe recall of events encompassing the past decade his score was extremely poor. Similarly, on tasks requiring him to name photographs of well-known people, or to order them in
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time, his performance was very severely impaired. When asked to match one of three spoken plausible alternatives to a photograph (i.e., using the names of three equally famous people) his score was not significantly better than chance. These findings replicate an earlier investigation using the identical stimulus material and procedures (Sanders & Warrington, 1971). In contrast on a revised version of the Famous Name Completion task described by Sanders and Warrington (1975) R.F.R. scored within the lower limits of the normal range while his ability to name the faces was severely impaired. Using a variant of a multiple choice recognition memory test in which one famous face was paired with two visually similar but unknown distractor items his performance was dramatically and unexpectedly good. Extending this procedure to the verbal domain his performance was at ceiling in selecting the famous name from a choice of three (two distractor items being similar unknown names). In these instances we have evidence that his word vocabulary for famous names and his visual vocabulary for famous faces was considerably greater than clinical observation or standard memory assessmentprocedures would indicate. These observations force us to reconsider the nature and extent of representations in event memory and their relationship to factual knowledge. Such findings could not easily be incorporated into any model of memory that assumes that there is a simple continuum between events and facts which is reflected by the relative preservation of overlearned and/or long-established “information” and the vulnerability of “events.” By such an account, any difference in performance on these tasks would be accounted for by differences in “trace strength” (e.g., Cohen & Squire, 1981). For R.F.R. there was evidence of discontinuities in his performance which are orthogonal to this dimension. First, there was the contrast between his impairment in recalling salient autobiographical or public events occurring throughout his adult life and his retained ability to define words which had been introduced into the language during the same period. This effect is far from being trivial to recapitulate: he could define AIDS but did not know that his mother had died. Second, there was a disproportionate gain in his recall of famous names using a “completion” technique. Third, he appeared to have a disproportionate difticulty in naming, ordering in time, or in discriminating between the names of famous personalities as compared with being able to identify the same stimulus items when asked to make a simple familiarity judgment. These findings together with the evidence for the selective preservation of event knowledge in patients with very impaired factual knowledge render untenable any interpretation of amnesia in terms of a simple continuum of declarative knowledge.
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The main alternative class of theory of amnesia emphasizesthe distinction between two or more qualitatively different types of representation for facts and/or events (Tulving, 1972; Warrington, 1975). This position has been developed in the disconnection hypothesis of amnesia (Warrington & Weiskrantz, 1982). Their formulation postulates that effective memory requires a continual interaction between factual knowledge and active cognitively mediated schemata. The present data showing a dissociation between R.F.R.‘s preserved new word vocabulary and his impaired recall of personally salient events is entirely compatible with such an account. We wish to go further and to suggest that this framework can also incorporate the other type of dissociation which we have observed namely between different methods of testing R.F.R.‘s knowledge of names and faces of famous people. Previous studies have emphasized the episodic/event aspect of memory for names and faces (e.g., Warrington & Sanders, 1971; Cermak & O’Connor, 1983). This position clearly requires modification since the present findings are indicative of a double (or possibly multiple) representation of such information. The level of representation which is “sampled” appears to differ systematically according to the type of task which is used. We would propose that name completion, as is the case for word completion tasks, can be achieved by relatively automatic processes within the lexical/semantic system itself. Similarly, simple familiarity judgments could also be achieved on the basis of processes operating solely within the fact memory system. In contrast, precise identification of, and discrimination between, names and faces of similar famous people requires access to information in active, continuously updated cognitive schemata. Thus names and faces of famous people may be represented in more than one system: both in a vocabulary-like fact memory system and in cognitively mediated schemata. Perhaps as was argued previously the integration of both sources of information is required for their voluntary recall (Warrington, 1986). The present findings indicate that “retrograde amnesia” is by no means a matter of simple univariate forgetting gradients but may be at least as complex in its characteristics as is anterograde memory loss. The present findings may go some way toward resolving the conflicting evidence regarding the severity and extent of retrograde amnesia in patients assessed on different remote memory tasks. It is clear that both the diagnosis of impairment and estimates of its magnitude depend not only on the material used for testing, but also upon the type of test which is used. The observation of a preserved “vocabulary” should not necessarily be considered as evidence that the patient has intact retrograde knowledge. Indeed, the present case R.F.R., has a dense retrograde amnesia which spares his vocabulary for famous names and his visual vocabulary for famous faces. It appears as though without access to or interaction with
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a more active cognitive mediational memory system, such information is functionally useless. APPENDIX Mrs. R.F.R. (2.12.86)
I
Mr. R.F.R. (3.12.86)
Q. Tell me all about your wedding? A. The anniversary is on the 10th while he A. I cannot remember very much about it, is in here. It was at St. Mark’s in Weybridge, not because of the drink I consumed I assure he may remember Father O’Leary who did you. I know it was a Catholic ceremony the service (. . .) We went to Paris on hon- which was rather alien to me because I am eymoon. Nothing much apart from that. not a Catholic. I was literally on edge (a) because I was getting married and (b) because of this. Q. Tell me about your first home? A. I cannot remember where we lived when A. It was a police maisonette in Weybridge. we first got married. There were 6 maisonettes for police. Quite a nice little home (. . .) We were there for about 18 months after we got married. Q. Tell me about all the cars you and R.F.R. have ever owned? A. When I first met him, Austin A35, I can A. I cannot even remember what car I’ve even remember the number of that. 278.SBG got at the moment. and that is going back over 20 years (. . .) a Corsair Estate and a Subaru the car he’s got at present. Q. Tell me about the medical problems you had with your first child? A. We had a slight accident when I was With Colin, there was something, I know there was something but I cannot remember about 1 or 2 months pregnant. Everything was going fine until, but I suffered from high what it was I’m afraid. blood pressure (. . . .) When Colin was born he had a “club” foot. Q. Tell me about Colin’s schooling and present job? A. Sutton junior school he started at. He A. His present job I can’t remember what was quite bright, no problems, very interested he is doing at the moment. His education I in football and sport and then he went to think it was just an ordinary standard edEpsom school (. . .) then he decided to do ucation. I don’t think he went to college or something else and R.F.R. went with him I don’t think he obtained any educational certificates, I mean matriculation certificates, to the Army Careers, the Airforce, the Navy, things like that. he preferred the Airforce.
APPENDIX
II: R.F.R.3 Autobiographies
1st Attempt Schooldays. I received a basic elementary school education until I reached the age of eleven years when I passed the entrance examination to a higher education college. I attended college until I was seventeen years old, leaving after passing the matriculation and Higher Schools certificates. Services. I was a regular short-service airman with the Royal Air Force, attached to
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the R.A.F. Photographic Intelligence Section. I spent most of my service time in the Middle East. I served at total of just under four years. Career. I specialised as soon as possible after completing my probationary period. I cannot got into detail as it is a subject classified as “secret” and covered by statute. I have served in various locations in the London area but most of my service has been with Scotland Yard. Marriage andfamily. I have been married for twenty-one years-which is in the region of twenty years longer than many people said the marriage would last! I have three children viz two boys, and a daughter.
7th Attempt Schooldays. I attended elementary school until the age of eleven years when I passed the scholarship examination and went on to grammar school. I attended grammar school until the age of seventeen years, leaving after matriculation etc. My specialised subject was foreign languages, i.e., French and German. Services. I was a regular (short-service) with the R.A.F. for a little over three and a half years. I served with the “Photographic Intelligence Section” of the service and spent most of my service in the Middle East (Egypt). Career. Recall virtually zero! Marriage and family. I married my wife in December 1966. We have three children, viz. two boys and a girl. We live in Sutton, in Surrey, in a “married quarters” property.
REFERENCES Albert, M. S., Butters, N., & Levin, J. 1979.Temporal gradients in the retrograde amnesia of patients with alcoholic Korsakoff’s disease. Archives of Neurology, 36, 21I-216. Cermak, L. S., & Butters, N. 1986. A case study of the forgetting of autobiographical knowledge: Implications for the study of retrograde amnesia. In D. C. Rubin (Ed.), Aufobiographical memory. Cambridge: Cambridge Univ. Press. Cermak, L. S., & O’Connor, M. 1983. The retrieval capacity of a patient with amnesia due to encephalitis. Neuropsychologia, 21, 213-234. Cohen, N. J., & Squire, L. R. 1981. Retrograde amnesia and remote memory impairment. Neuropsychologia,
19, 337-356.
Coughlan, A. K., & Warrington, E. K. 1981. The impairment of verbal semantic memory: A single case study. Journal of Neurology, Neurosurgery and Psychiatry, 44, 10791083. Crovitz, H. F., & Schiffman, H. 1974. Frequency of episodic memories as a function of their age. Bulletin of the Psychonomic Society, 4, 517-518. Marslen-Wilson, W. D., & Teuber, H. L. 1975. Memory for remote events in anterograde amnesia: Recognition of public figures from news photographs. Neuropsychologia, 13, 353-364. McCarthy, R. A., & Warrington, E. K. 1986.Phonological reading: Phenomena and Paradoxes. Cortex,
22, 359-380.
McCarthy, R. A., & Warrington, E. K. 1987. The Double Dissociation of short-term memory for lists and sentences: Evidence from Aphasia. Brain, 110, 1545-1563. McKenna, P., & Warrington, E. K. 1980. Testing for nominal dysphasia. Journal of Neurology, Neurosurgery and Psychiatry, 43, 781-788. Meudell, P. R., Mayes, A. R., & Neary, D. 1981. Amnesia is not caused by cognitive slowness. Cortex, 16, 413-419. Parkin, A. J. 1984. Amnesic syndrome: A lesion-specific disorder. Cortex, 20, 479-508. Sanders, H. I., & Warrington, E. K. 1971. Memory for remote events in amnesic patients. Brain,
94, 661-668.
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AND MC CARTHY
Sanders, H. I., & Warrington, E. K. 1975. Retrograde amnesia in organic amnesic patients. Cortex, 11, 397-400. Squire, L. R., Cohen, N. J., & Nadel, L. 1984. The medial temporal region and memory consolidation: A new hypothesis. In H. Weingartner & E. S. Parker (Eds.), Memory consolidation: Psychobiology of cognition. Hillsdale, NJ: Erlbaum. Tulving, E. 1972. Episodic and semantic memory. In E. Tulving & W. Donaldson (Eds.), Organization of memory. New York: Academic Press. Tulving, E. 1983. Elements of episodic memory. London/New York: Oxford Univ. Press (Clarendon). Warrington, E. K. 1975. The selective impairment of semantic memory. Quarter/y Journal of Experimental Psychology, 27, 635-657. Warrington, E. K. 1982. Neuropsychological studies of object recognition. Philosophical Transactions of the Royal Society of London B, 298, 15-33. Warrington, E. K. 1984. Recognition memory test. Windsor Berks.: NFER-Nelson. Warrington, E. K. 1986. Memory for facts and memory for events. British Journal of Clinical Psychology, 25, I - 12. Warrington, E. K., & Sanders, H. I. 1971. The fate of old memories. Quarter/y Journal of Experimental Psychology, 23, 432-442. Warrington, E. K., & Weiskrantz, L. 1974. The effect of prior learning on subsequent retention in amnesic patients. Neuropsychologin, 12, 419-428.k Warrington, E. K., & Weiskrantz, L. 1982. Amnesia: A disconnection syndrome? Neuropsychologiu, 20, 233-249. Weiskrantz, L. 1985. On issues and theories of the human amnesic syndrome. In N. M. Weinberger, J. L. McGaugh, & G. Lynch (Eds.), Memory sysrems of the bruin. New York: Guilford Press. Whiteley, A. M., & Warrington, E. K. 1978. Selective impairment of topographical memory: A single case study. Journal of Neurology, Neurosurgery and Psychiatry, 41, 575578.
AND
COGNITION
7, 184-200 (1988)
The Fractionation of Retrograde Amnesia ELIZABETH
K. WARRINGTON AND ROSALEEN A. MCCARTHY
National
Hospital,
Queen Square, London
WCIN 3BG
This single case study describes our investigations of the retrograde memory deficit of a patient who became severely and selectively amnesic after an encephalitic illness. On clinical assessment his retrograde deficit for both personal and public events appeared to encompass his entire adult life. However, he retained knowledge of words introduced into the vocabulary during the retrograde period. The experimental investigation documented his inability to recall, recognize, and place in temporal order the names and faces of famous people for all time periods sampled. By contrast, his recall of either a famous face or a famous name was significantly facilitated by the verbal cue of the person’s first name and initial of the surname (i.e., Margaret T . .). His performance on a test of “familiarity” that required him to select the famous name or the famous face from two distracters (unknown) was within normal limits. It is argued that names and faces of famous people are represented in more than one system: both in a vocabulary-like fact memory system that is preserved and also in a cognitively mediated schemata that in this case is functionally inoperative. 0 1988 Academic Press, Inc.
Since Korsakoff’s classical observations, long periods of retrograde amnesia have presented the psychologist and neurologist alike with a conundrum. On the one hand very long periods of retrograde amnesia for events have been reported, stretching in some instances through the individual’s entire life span. At the same time such syndromes can be associated with preserved knowledge of factual information, some of which may have been acquired during the retrograde period. This has given rise to debate as to whether retrograde memories and factual memories are on some continuum only differing in trace strength, or alternatively We thank Dr. G. Stern, Department of Neurology, University College Hospital, London, for referring R.F.R. to this department for psychological assessment. We are also grateful to Dr. P. C. Gautier-Smith for arranging his admission to the National Hospital for further investigations. We thank Chris Brown for her assistance in testing the control subject. Rosaleen McCarthy’s research is supported by the University of Cambridge; her present address is Department of Experimental Psychology, University of Cambridge, Downing Street, Cambridge, CB2 3EB, England. Address reprint requests to Prof. Elizabeth K. Warrington, National Hospital, Queen Square, London, WClN 3BG, England. 184 0278-2626/88$3.OO Copyright All rights
0 1988 by Academic Press, Inc. of reproduction in any form reserved.
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whether they implicate the involvement of two relatively independent subsystems. Those who view memory for facts and memory for events as forming a continuum would argue that the information that amnesics are able to recall is highly overlearned and/or has the status of procedural knowledge. The probability of item recall is therefore postulated to be a function of “trace strength.” To support this notion of a continuum they would cite evidence that in some severe amnesic patients subtle deficits in the processing of factual information can be demonstrated. Thus it is argued that a continuum can be demonstrated between recently acquired information which cannot be retrieved at all, and more distant information for which the deficit is much less obvious (e.g., Cohen & Squire, 1981; Squire, Cohen, & Nadel, 1984).However, impairments in factual knowledge processing are by no means a necessary concomitant of amnesia. Thus both Meudell, Mayes, and Neary (1981), and Warrington and Weiskrantz (1982) reported evidence from a series of R.T. experiments which indicated that amnesics were not significantly different from control subjects in their ability to access category exemplars and antonyms. Indeed such evidence has been interpreted as favoring a discontinuity between memory for facts and memory for events (e.g., Tulving, 1983). More direct evidence for discontinuity may be adduced from patients with profound deficits affecting certain aspects of factual memory, who can in no sense be regarded as having an amnesic syndrome. Warrington (1975) described three patients with progressive degenerative cortical pathology in whom knowledge of both visual and verbal factual information was selectively impaired. At the same time their memory for ongoing events (within the constraints imposed by their loss of factual knowledge) appeared to be satisfactory (Warrington, 1975). One of these patients was formally tested and was shown to score at a near normal level on verbal learning tasks on which amnesic patients failed (Coughlan & Warrington, 1981). We have since investigated two further cases with this syndrome both of whom had profound and widespread impairments such that their verbal vocabulary was reduced to the most rudimentary level. (McCarthy & Warrington, 1986 and 1987). Nevertheless, both patients were employed in full-time jobs which necessitated working without supervision (which is clearly beyond the abilities of patients with a global amnesic syndrome). Since the issue of continuity versus discontinuity hinges upon the properties of retrograde amnesia, the question arises as to how best to specify this deficit (or deficits). Commonly the quantitative investigation of this problem has tested the knowledge of public events and personalities antedating the illness, which has the advantage of providing an objective measure of memory. However, such techniques have proven somewhat problematic, in that baseline “normal” forgetting curves have differed between investigations, thereby resulting in different estimates
186
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of memory loss in the amnesic patient (see Cermak & Butters, 1986 for a full discussion of this issue). Thus in the original investigation using these methods, negatively accelerated age-related serial position curves were obtained in a large standardization sample, (Warrington & Sanders, 1971), while amnesic patients showed an apparently absolute deficit for all time periods sampled (Sanders & Warrington, 1971). When questions and testing procedures are adjusted so that amnesic patients do not have an absolute deficit, control subjects no longer show the expected forgetting function (Albert, Butters, & Levin, 1979). It is now widely accepted that such techniques are vulnerable to many sources of artifact (Weiskrantz, 1985) and more recent evidence appears to suggest that they may give a misleading and/or incomplete estimate of the amnesic patients’ residual capacities for “remembering” remote events (Cermak & O’Connor, 1983). We have recently had the opportunity to investigate an amnesic patient whose memory for both recent and more distant events was severely impaired. In this report we describe a series of tests designed to manipulate different methods of testing retention for events which spanned his adult life. To this end we investigated his ability to recognize, recall, describe, and identify well-known people, using verbal and visual material. We have been able to document a number of unexpected task-dependent dissociations suggesting that there may be multiple long-term memory representations for this class of information. We will argue that our findings are incompatible with any simplistic continuum model of retrograde memory loss. CASE HISTORY R.F.R. was a 54-year-old (15.3.32) police officer who was admitted to the National Hospital Queen Square on 2.12.86 for further investigations of his severe and persistent memory difficulties. In July 1985 R.F.R. had suffered a pyrexial illness and became extremely confused. This was followed by a lowering in his level of consciousness and he was admitted to the Royal Free Hospital under the care of Dr. Harban where he was observed to be comatose. A lumbar puncture was performed and he had a white cell count of 150 with 95% lymphocytes. A C.T. scan at this stage was normal and his EEG showed mild diffuse abnormalities. He was treated with acyclovir and steroids. His level of consciousness gradually improved but it then became evident that he had a severe anterograde and retrograde amnesia. A repeat C.T. scan (23.1.87) demonstrated asymmetrical areas of low attenuation confined to both temporal lobes with extensive damage in the right temporal region, and in the left temporal lobe the abnormal region was confined to the medial surface (McCarthy & Warrington, in preparation). He was considered to have suffered a herpes simplex encephalitis.
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OF RETROGRADE
AMNESIA
187
PSYCHOLOGICAL TEST FINDINGS R.F.R. was originally tested on the WAIS in August 1985 and he obtained a verbal IQ of 117 and a performance IQ of 99. He was reassessed in January 1986 by which time his verbal IQ had improved to 128 and his performance IQ to 110. He obtained a reading IQ equivalent of 120 which is in good accord with his verbal IQ but suggeststhat his performance IQ might be slightly below his optimal level. On specific tests of language function his performance was entirely satisfactory. He had no difficulty whatever in completing a shortened version of the token test of language comprehension. He scored 145/150 correct on the Peabody Picture Vocabulary Test. He scored at an average level on a stringent graded difficulty naming test (McKenna & Warrington, 1980). His explanation of proverbs was satisfactory. His verbal fluency was excellent (a task he approached using very efficient “alphabetic” strategies) for example in 1 min he was able to generate 20 words beginning with the letter “b,” 21 words beginning with the letter “s,” 15 boys names, 16 occupations, and 24 animals. His perceptual and spatial skills appeared to be intact he was able to identify 20/20 incomplete letters and 19/20 unusual view photographs, and scored 18/20 on a same/different face matching test (Warrington, 1982). He also scored within the normal range on tests of spatial discrimination and cube analysis (Whiteley 8z Warrington, 1978). In contrast to his well-preserved intellectual, language, and perceptual abilities he was profoundly and severely amnesic. Thus he was totally unable to maintain any record of ongoing events, he was completely disoriented in time and place, and he was quite unable to give an account of his present circumstances. Not only was there evidence of a marked anterograde memory deficit, but there was also evidence of a severe retrograde deficit stretching into the remote past. On formal memory testing he scored at a chance level on two parallel forms of the verbal and visual recognition memory tests (Warrington, 1984). He scored 31/50 and 27/50 on the verbal versions and 32/50 and 26/50 on the visual versions. On a three-choice recognition memory test for colored photographs of Camden scenes he scored 8/30. On a verbal paired associate learning test his performance was markedly impaired scoring 8/24 and he showed no improvement with a second attempt 6/24. His scores were at a worse level than the poorest control (C. Brown, personal communication). Likewise his story recall (Wechsler Memory Scale) was severely impaired even on immediate recall. On the memory for designs test (WMS) his recall was fragmentary in the extreme. In summary R.F.R. presents with an exceptionally selective and severe amnesia. His cognitive abilities have been shown to be well preserved whereas there is a dense and profound anterograde and retrograde memory
188
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loss. In this report we focus on his retrograde memory deficit: first reporting a clinical description and second our experimental investigations.
CLINICAL DESCRIPTION OF RFR’s RETROGRADE AMNESIA R.F.R.‘s retrograde amnesia affected both personal and public events stretching into the remote past. Indeed he was unable to give a detailed or coherent account of any episode from either domain. Although he was able to provide a skeleton autobiography it was sparse, having the characteristics of a mere outline lacking in real substance. On questioning he was unable to elaborate on specifc points. He appeared to have little memory for many of the most salient events in a person’s life. For example, he knows that he was stationed in Egypt during his service with the R.A.F. but he commented “I am not sure if I got to Cairo.” Asked about his honeymoon he replied “Europe somewhere, don’t know where.” Given the choice Brussels, Paris, Rome, he said “not Rome I don’t think I have been to Rome, I have an affection for Paris, so it must have been Paris I guess.” He does not appear to realize that his mother died 6 years ago. As for public events he claims he can recall nothing at all. The whole tenor of his conversation is pervaded by uncertainty and repetitiveness and he was to some extent aware of this: for example, in the course of half an hour he might say half a dozen times “I have probably told you a hundred times that I have a very high DRAG rating, I’m sorry I don’t mean to bore you.” He was shown a number of family photographs presented out of context from albums provided by his wife. A number of notable failures occurred. Although he usually recognized photographs of his children he failed to recognize them when they were younger. Even pictures taken 4 or 5 years ago were not always recognized. He hesitantly recognized his mother in several photographs. On one occasion he failed to identify his grandparents. Longstanding friends and colleagues were all strangers to him. Perhaps most telling were his failures to recognize both recent and older photographs of his wife. Structured
Interview
We interviewed both R.F.R. and his wife putting the same questions, spanning the period of their marriage, to each. These questions probed the major salient events of their lives during the last 20 years. R.F.R.‘s responses were very sparse by comparison with his wife’s (see samples in Appendix 1). Autobiographical
Memory
On seven separate occasions R.F.R. was asked to write an account of his life using the following headings: (a) Schooldays, (b) Time in the services, (c) Career with police, (d) Marriage and family. He was en-
FRACTIONATION
OF RETROGRADE
AMNESIA
189
couraged to take his time and provide as much detail as he could. The first and final of these accounts are given in full in Appendix 2. His five intervening accounts were substantially identical (down to the level of the specific vocabulary which was used). His descriptions under each heading are very brief indeed and all these skeletal accounts appeared to be retrieved with difficulty. They have many of the characteristics of those memories described as “personal semantics” by Cermak and O’Connor (1983). On no occasion did he recall having previously been asked to write such an account. Probe Word Recall
The Crovitz and Schiffman (1974) technique was used to elicit memories from his past life. Three of his responses to 22 key words suggested that he was recalling a specific rather than a generic event. One of his more precise responses was to the word “tree.” “As a child I was . . . a youth . . . reprimanded by my mother for climbing one of the trees in the back garden . . . . Three trees and the middle one had a branch which came up horizontally, 18 feet above the ground. I used to perch on the tree. I remember having conversations with the boy in the next garden while sitting on this branch.” Public Events
He was asked 20 questions about major events of the last 15 years. He was only able to give an adequate reply to one of these (viz.) who are the boat people). Seven age-matched controls obtained a mean score of 15 (range 1l-20 correct). New Word Vocabulary
His ability to define a “new word” word vocabulary stands in striking contrast to his otherwise dense retrograde amnesia. He was asked to define 50 new words and company names that have come into the (English) vocabulary within the last 20 years. Some examples are as follows: Provisionals-members of the IRA a form of terrorist organization intent on unifying Ireland. AIDS-illness or disease-the aids virus. Thatcherism-word applied to the policies adopted by Margaret Thatcher. Ultraconservatism basically a conservative policy. Shuttle-space shuttle-passenger carrying spaceship-not just a rocket it’s for both landing and re-taking off. Telecom-British telecom organization responsible for communication, telephones telegrams, etc.-Nationalized. His only error in the entire corpus was to define “Telecom” as Nationalized rather than Privatized.
190 EXPERIMENTAL
WARRINGTON
AND
INVESTIGATION
MC CARTHY
OF RETROGRADE
AMNESIA
Experiment 1 In an investigation of retrograde amnesia, comparing naming and recognition of photographs of contemporary personalities with personalities who had faded from view at various time periods in the past, Sanders and Warrington (1971) found that amnesic patients showed marked impairments at all time periods sampled on both versions of the task. Using identical stimuli and procedures R.F.R. was tested on items from the three most recent time periods investigated in that study: namely, 15 contemporary personalities (in the forefront of the news in the late 196Os), 15 personalities who had faded from view by the early 1960s and 15 personalities who had faded from view by the second half of the 1950s). He was first asked to identify each personality and in the event of failure he was given three choices: the target name together with two equally famous distractor names. Contemporary control data was obtained using 10 age-matched male controls (hospital staff). Results The percentage correct for R.F.R. and the mean percentage correct for the control group are given in Table 1. In the control group there was a small decrement in performance related to the remoteness of the famous person. For this stimulus material, on the recognition version of the task, their performance was near to ceiling. In contrast R.F.R. only succeeded in identifying 1 of these 45 personalities and in the recognition version of this task his performance was not significantly different from chance. Comment It is generally accepted that in amnesia due to Wemike-Korsakoff encephalopathy there may be long periods of retrograde amnesia. However, there has been some debate as to the presence of retrograde impairments in amnesia due to medial temporal lobe damage (see Parkin, 1984 for review). R.F.R., like one of the original cases reported by Sanders and Warrington, has damage to the medial surface of the temporal lobes but nevertheless shows evidence of a severe retrograde impairment on this naming and recognition test for faces of famous personalities. EXPERIMENT
2
Cued recall and/or word completion techniques have been shown to have robust facilitatory effects for amnesic patients. In this context it is of some interest to note that those studies claiming that there may be a considerable degree of retrograde memory preservation in some amnesics have tested the recall of retrograde “memory” using cueing techniques
x = 11.5 SD = 2.12
2 SD = 2.98
SD = < I
R. F. R. Controls (N = IO)
Naming photograph with cue
Generating name from auditory cue
R. F. R.
Controls (N = 10) R. F. R. Controls (N = 10)
Naming Photograph
TABLE 2
1 z = 7.75
Recall 7 x = 13.1 SD = I.51
Recognition
Time period early 1960s
7 x = 14.9
Recognition
Late 1960s
SD = 2.68
0 x = 5.25
Recall
x == 8.7 SD 3.6 II x = 14.0 SD = 1.34 I2 2 = 8.7 SD = 3.21
0
Contemporary personality
SD =
x =
SD =
I3 6.8 1.5
2.05
6.8 2.89 9 x = 11.3
x == SD
I
Mid-1970s
Time Period
SD =
x =
SD =
2.92
II 5.5
2.33
6.3 2.68 7 x = 11.4
2 == SD
1
Mid- to late-1960s
SD = < 1
5 x=11.9
Recognition
Late 1950s
CUEING RECALL OF NAMES OF PHOTOGRAPHSOF FAMOUS PEOPLE AND GENERATING THESE NAMES FROM AN AUDITORY CUE
R. F. R. Age-matched controls (N = 8)
Recall
TABLE I RECALL AND RECOGNITION OF FAMOUS FACES
F
E
Ei
F 1’1
2 ZI
R
2 0 crl
2
5 5
2
192
WARRINGTON
AND MC CARTHY
but do not systematically differentiate between those memories retrieved in “naming” or “cued” conditions (e.g., Albert et al., 1979). Our aim in this experiment was to attempt to replicate the early observations of a dissociation between “cueing” and “naming” conditions (MarslenWilson & Teuber, 1975; Sanders & Warrington, 1975) in a patient in whom a particularly severe retrograde impairment has been demonstrated. Procedure The stimulusmaterialconsistedof photographsof public figures.Fifteensetsof three personalitieswho hadbeenfamiliarin oneof two time periodsand had since faded from public view (mid-1970s mid-to late-l%Os) together with one contemporary figure were constructed. The three individuals comprising each set were closely matched for occupational status and importance, e.g., David Steele, Jeremey Thorpe, and Jo Grimmond (Liberal party leaders); Len Murray, Vie Feather, and George Woodcock (Trades Union Leaders). R.F.R. was asked to name each personality and when unable to do so he was asked to retrieve the person’s surname when provided with the Christian name and the inital letter of the surname. On a subsequent testing session he was presented with the Christian name and initial letter of each of surnames of each of the 45 personalities and asked to generate/guess the appropriate famous name. For both the pictorial and auditory conditions the 45 photographs were presented in a pseudo-random order with regard to both era and personality “types.” Two independent age-matched control groups were tested; 10 on the visual and 6 on the verbal version of the task.
Results The percentage correct for the naming task and for each of the cuing conditions is given in Table 2. R.F.R. is far worse than the poorest control in the naming task; however, he performed at a level equivalent to the controls in the photograph + cue condition and was better than control subjects when asked to guess or generate any famous name on the basis of the verbal cue alone. Comment These findings replicate the original findings of Sanders and Warrington (1975) in showing a significant facilitatory effect of cuing in naming famous people. Clearly the very robust word completion effects obtained in many investigations of amnesic patients are not necessarily confined to material which is a component of long established linguistic representations (e.g., words acquired in the course of language development). In this experiment we have established that such word completion effects may be at least as powerful for a proper name vocabulary acquired relatively recently (during the last 5 to 15 years), and certainly for a vocabulary learned well within the period for which he has a “retrograde amnesia.” Our two groups of matched control subjects found the photograph + cue version of the task somewhat easier than the “cue alone” condition. We would not wish to claim that there was a reversal of this effect for R.F.R. insofar as he may have benefited from prior exposure in the visual +
FRACTIONATION
OF RETROGRADE AMNESIA
193
cue condition. Nevertheless we would claim that this pattern of results suggests that the cueing condition was eliciting items from his vocabulary, rather than simply facilitating retrieval from a weak trace. Some implications of these findings will be discussed below. EXPERIMENT
3
In Experiment 2 in which we investigated word completion effects of well-known peoples names with and without a photograph of the individual, there was evidence of considerable implicit knowledge of public figures, but at the same time little evidence of any explicit knowledge insofar as in the naming condition he was very markedly impaired. The question therefore arises as to whether his impairment on such tasks was dependent upon the requirement to verbalize his responses. To this end we explored his ability to place photographs and names of public figures in their appropriate temporal order. Procedure Two groups of five normal subjects were tested on tasks requiring them to pick out the most contemporary and the most remote personality, one group being tested with a face stimulus and the other with a spoken name. On the basis of their performance a subset of 10 items was selected on which the number of items totally correct was relatively high (88% for the visual version and 82% for the auditory version). These items were given to R.F.R. first for ordering of the photographs and second for ordering of the spoken names.
Results This task, which was designed to give a near ceiling effect with normal subjects, was extremely difficult for R.F.R. He was only able to order two of the photographs sets correctly and to order only one of the spoken name sets correctly. This level of performance is no better than that which would be expected by chance. Comment This experiment indicates that R.F.R.‘s retrograde amnesia extends to tasks without an explicit verbal component. These findings, at the very least, provide evidence for a dissociation between names and faces as entries in a vocabulary-like system and names and faces as “temporal” events. This dissociation will be discussed in greater detail below. EXPERIMENT
4
In Experiment 2 using cueing techniques we demonstrated that R.F.R. retained his vocabulary for a number of names of public figures from the recent past. The aim of this experiment was to obtain further evidence of R.F.R.‘s visual and verbal “vocabulary” for famous personalities using a measure of verbal and visual name and face familiarity.
194
WARRINGTON
AND MC CARTHY
FIG. I. Examples of face familiarity test stimuli with one famous face and two unknown distractor items.
Method Two sets of 15 names and photographs of famous people were assembled; one set was of personaIities who were prominent in the early 198Os,the other of people who had been most famous approximately 10 to 15 years previously, and who had since faded from prominence. In the verbal version each famous name was paired with two unknown, but “similar” distractor items (e.g., Shirley Williams, Joan Ingham, and Christine Sandys; Ian Paisley, Frank Smith, and Stan Hughes). Correct responses were followed by a request for the individual’s name. In the visual version photographs of unknown people who were somewhat similar in appearance were used (see Fig. I). R.F.R. was asked to indicate which was the famous name or face from arrays or lists of three items (the target and two distractors) in which the target item occurred equally often in each position. The visual version was presented on 1 day, and the auditory version was tested on a subsequent occasion. Eight age-matched controls were tested on the visual version of the task.
FRACTIONATION
195
OF RETROGRADE AMNESIA TABLE 3
FACE AND NAME
FAMILIARITY
TEST
Time period 1980-1985 Face naming
R. F. R. Controls (N = 8)
Face selection
R. F. R. Controls (N = 8)
Name selection
R. F. R.
2
x = to.1 SD =
2.93 13 2 = 13.25 SD = 1.47
15
1970-1980 1 8.1 2.6 12 x = 13.75 SD = 1.28 14
? = SD =
Results The percentage correct for R.F.R. on both the visual and the verbal versions of the task and for the matched control group on the visual version is given in Table 3. R.F.R.‘s level of performance was at the lower limits of normal on the visual version and he made only one error on the verbal version. Comment R.F.R.‘s performance on this task is exceptionally good considering his very impaired performance on tasks requiring him to match a photograph of a famous person to one of three equally famous spoken names. Taken together with his performance on the name completion task these findings provide direct evidence that he not only has a famous name vocabulary, but that he also has a famousface vocabulary. He therefore has preserved ability to make familiarity judgments on a class of material which has hitherto provided the archetypal stimulus material for testing retrograde amnesia. Discussion
In this series of experiments we have reported our investigations of a severely amnesic patient whose intellectual and cognitive skills were otherwise entirely satisfactory. In this account we have focused on the retrograde component of his global memory deficit. In our clinical case report we document the pervasive and dense nature of his retrograde amnesia. On the basis of structured interviews and his own written autobiographical accounts his deficit appeared, at the very least, to encompass his entire adult life. Despite this exceptionally severe retrograde deficit, there was evidence that R.F.R. was able to recall a new word vocabulary (e.g., AIDS) which was acquired during the same period. On a questionnaire designed to probe recall of events encompassing the past decade his score was extremely poor. Similarly, on tasks requiring him to name photographs of well-known people, or to order them in
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time, his performance was very severely impaired. When asked to match one of three spoken plausible alternatives to a photograph (i.e., using the names of three equally famous people) his score was not significantly better than chance. These findings replicate an earlier investigation using the identical stimulus material and procedures (Sanders & Warrington, 1971). In contrast on a revised version of the Famous Name Completion task described by Sanders and Warrington (1975) R.F.R. scored within the lower limits of the normal range while his ability to name the faces was severely impaired. Using a variant of a multiple choice recognition memory test in which one famous face was paired with two visually similar but unknown distractor items his performance was dramatically and unexpectedly good. Extending this procedure to the verbal domain his performance was at ceiling in selecting the famous name from a choice of three (two distractor items being similar unknown names). In these instances we have evidence that his word vocabulary for famous names and his visual vocabulary for famous faces was considerably greater than clinical observation or standard memory assessmentprocedures would indicate. These observations force us to reconsider the nature and extent of representations in event memory and their relationship to factual knowledge. Such findings could not easily be incorporated into any model of memory that assumes that there is a simple continuum between events and facts which is reflected by the relative preservation of overlearned and/or long-established “information” and the vulnerability of “events.” By such an account, any difference in performance on these tasks would be accounted for by differences in “trace strength” (e.g., Cohen & Squire, 1981). For R.F.R. there was evidence of discontinuities in his performance which are orthogonal to this dimension. First, there was the contrast between his impairment in recalling salient autobiographical or public events occurring throughout his adult life and his retained ability to define words which had been introduced into the language during the same period. This effect is far from being trivial to recapitulate: he could define AIDS but did not know that his mother had died. Second, there was a disproportionate gain in his recall of famous names using a “completion” technique. Third, he appeared to have a disproportionate difticulty in naming, ordering in time, or in discriminating between the names of famous personalities as compared with being able to identify the same stimulus items when asked to make a simple familiarity judgment. These findings together with the evidence for the selective preservation of event knowledge in patients with very impaired factual knowledge render untenable any interpretation of amnesia in terms of a simple continuum of declarative knowledge.
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The main alternative class of theory of amnesia emphasizesthe distinction between two or more qualitatively different types of representation for facts and/or events (Tulving, 1972; Warrington, 1975). This position has been developed in the disconnection hypothesis of amnesia (Warrington & Weiskrantz, 1982). Their formulation postulates that effective memory requires a continual interaction between factual knowledge and active cognitively mediated schemata. The present data showing a dissociation between R.F.R.‘s preserved new word vocabulary and his impaired recall of personally salient events is entirely compatible with such an account. We wish to go further and to suggest that this framework can also incorporate the other type of dissociation which we have observed namely between different methods of testing R.F.R.‘s knowledge of names and faces of famous people. Previous studies have emphasized the episodic/event aspect of memory for names and faces (e.g., Warrington & Sanders, 1971; Cermak & O’Connor, 1983). This position clearly requires modification since the present findings are indicative of a double (or possibly multiple) representation of such information. The level of representation which is “sampled” appears to differ systematically according to the type of task which is used. We would propose that name completion, as is the case for word completion tasks, can be achieved by relatively automatic processes within the lexical/semantic system itself. Similarly, simple familiarity judgments could also be achieved on the basis of processes operating solely within the fact memory system. In contrast, precise identification of, and discrimination between, names and faces of similar famous people requires access to information in active, continuously updated cognitive schemata. Thus names and faces of famous people may be represented in more than one system: both in a vocabulary-like fact memory system and in cognitively mediated schemata. Perhaps as was argued previously the integration of both sources of information is required for their voluntary recall (Warrington, 1986). The present findings indicate that “retrograde amnesia” is by no means a matter of simple univariate forgetting gradients but may be at least as complex in its characteristics as is anterograde memory loss. The present findings may go some way toward resolving the conflicting evidence regarding the severity and extent of retrograde amnesia in patients assessed on different remote memory tasks. It is clear that both the diagnosis of impairment and estimates of its magnitude depend not only on the material used for testing, but also upon the type of test which is used. The observation of a preserved “vocabulary” should not necessarily be considered as evidence that the patient has intact retrograde knowledge. Indeed, the present case R.F.R., has a dense retrograde amnesia which spares his vocabulary for famous names and his visual vocabulary for famous faces. It appears as though without access to or interaction with
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a more active cognitive mediational memory system, such information is functionally useless. APPENDIX Mrs. R.F.R. (2.12.86)
I
Mr. R.F.R. (3.12.86)
Q. Tell me all about your wedding? A. The anniversary is on the 10th while he A. I cannot remember very much about it, is in here. It was at St. Mark’s in Weybridge, not because of the drink I consumed I assure he may remember Father O’Leary who did you. I know it was a Catholic ceremony the service (. . .) We went to Paris on hon- which was rather alien to me because I am eymoon. Nothing much apart from that. not a Catholic. I was literally on edge (a) because I was getting married and (b) because of this. Q. Tell me about your first home? A. I cannot remember where we lived when A. It was a police maisonette in Weybridge. we first got married. There were 6 maisonettes for police. Quite a nice little home (. . .) We were there for about 18 months after we got married. Q. Tell me about all the cars you and R.F.R. have ever owned? A. When I first met him, Austin A35, I can A. I cannot even remember what car I’ve even remember the number of that. 278.SBG got at the moment. and that is going back over 20 years (. . .) a Corsair Estate and a Subaru the car he’s got at present. Q. Tell me about the medical problems you had with your first child? A. We had a slight accident when I was With Colin, there was something, I know there was something but I cannot remember about 1 or 2 months pregnant. Everything was going fine until, but I suffered from high what it was I’m afraid. blood pressure (. . . .) When Colin was born he had a “club” foot. Q. Tell me about Colin’s schooling and present job? A. Sutton junior school he started at. He A. His present job I can’t remember what was quite bright, no problems, very interested he is doing at the moment. His education I in football and sport and then he went to think it was just an ordinary standard edEpsom school (. . .) then he decided to do ucation. I don’t think he went to college or something else and R.F.R. went with him I don’t think he obtained any educational certificates, I mean matriculation certificates, to the Army Careers, the Airforce, the Navy, things like that. he preferred the Airforce.
APPENDIX
II: R.F.R.3 Autobiographies
1st Attempt Schooldays. I received a basic elementary school education until I reached the age of eleven years when I passed the entrance examination to a higher education college. I attended college until I was seventeen years old, leaving after passing the matriculation and Higher Schools certificates. Services. I was a regular short-service airman with the Royal Air Force, attached to
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the R.A.F. Photographic Intelligence Section. I spent most of my service time in the Middle East. I served at total of just under four years. Career. I specialised as soon as possible after completing my probationary period. I cannot got into detail as it is a subject classified as “secret” and covered by statute. I have served in various locations in the London area but most of my service has been with Scotland Yard. Marriage andfamily. I have been married for twenty-one years-which is in the region of twenty years longer than many people said the marriage would last! I have three children viz two boys, and a daughter.
7th Attempt Schooldays. I attended elementary school until the age of eleven years when I passed the scholarship examination and went on to grammar school. I attended grammar school until the age of seventeen years, leaving after matriculation etc. My specialised subject was foreign languages, i.e., French and German. Services. I was a regular (short-service) with the R.A.F. for a little over three and a half years. I served with the “Photographic Intelligence Section” of the service and spent most of my service in the Middle East (Egypt). Career. Recall virtually zero! Marriage and family. I married my wife in December 1966. We have three children, viz. two boys and a girl. We live in Sutton, in Surrey, in a “married quarters” property.
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