Profound Retrograde Amnesia Following Mild Head Injury: Organic or Functional?

PROFOUND RETROGRADE AMNESIA FOLLOWING MILD HEAD INJURY: ORGANIC OR FUNCTIONAL? Sarah Mackenzie Ross (University College London)

ABSTRACT This paper describes a 56 year old female patient (JJ) who suffered a minor head injury at work and presented with profound retrograde amnesia for both public events and autobiographical material spanning her entire life. In addition, she complained of wordfinding difficulties and anterograde memory impairment and neuropsychological assessment found evidence of mild executive dysfunction. Neurological investigations (CT and EEG) were essentially normal although changes indicative of small vessel disease were noted on MRI brain scan. Various forms and aetiologies of remote memory loss were considered including, simulated, psychogenic and organic amnesia, but differential diagnosis proved difficult. It is proposed that criteria used in clinical practice to differentiate functional and organic complaints are limited and this may be because (1) both factors can be involved in the aetiology of amnesia, and (2) a similar underlying brain mechanism, such as a retrieval deficit could underlie many instances of organic and psychogenic amnesia. Future research, complemented by functional brain imaging, is needed to explore the nature of retrieval deficits. Key words: retrograde amnesia, organic amnesia, functional amnesia, head injury

INTRODUCTION Impaired memory functioning is one of the most common symptoms following any kind of brain damage or disease and is a major cause of disability (Baddeley, 1990). Studies of amnesic patients have shown that memory is not a unitary system, but consists of different components which may be damaged independently (McCarthy and Warrington, 1992; Stracciari, Ghidoni, Guarino et al., 1994; De Renzi, Liotti and Nichelli, 1987). The distinction between anterograde and retrograde amnesia is a good example of this and has been used as evidence for the independence of mechanisms subserving these memory processes. Anterograde amnesia (loss of memory for events post injury or illness) is a common consequence of brain damage, but retrograde amnesia (loss of memory for events prior to the onset of illness or injury) is not always present, or may be transient, mild or temporally limited (Baddeley, 1990). Retrograde amnesia, usually involving the minutes, sometimes hours and more rarely days preceding brain damage is a common consequence of mild to moderate head injury (Lezak, 1995). Remote memory loss affecting months or at most a few years has been observed in patients who have undergone electroconvulsive therapy (Squire, Slater and Chace, 1975, 1976; Cohen and Squire, 1981). Retrograde amnesia which is temporally graded (i.e. distant Cortex, (2000) 36, 521-537

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memories are spared) has consistently been demonstrated in patients with Korsakoff syndrome (Butters, 1985; Kopelman, 1989a); in some patients with acute diencephalic damage as a result of bilateral thalamic infarct (Hodges and McCarthy,1993); and in patients who have sustained basal forebrain lesions. It has also been observed in patients with transient global amnesia (Hodges and Ward, 1989). Extensive retrograde amnesia affecting recall of past events without evidence of a temporal gradient (flat profile) has been observed in patients suffering from herpes simplex encephalitis, multiple sclerosis, subcortical dementias, frontal lobe dementia and in some patients with dementia of Alzheimer’s type (Hodges, 1995). Studies of amnesic patients indicate that damage to the CA1 fields of the hippocampus causes anterograde amnesia and a very limited retrograde amnesia (Zola Morgan, Squire and Amaral, 1986) whereas more widespread damage to medial temporal lobe and diencephalic structures results in temporally graded amnesia which is thought to be secondary to consolidation and retrieval deficits. Retrograde amnesia which is not temporally graded is associated with diffuse neocortical damage (Squire, 1992) rather than localised damage and is thought to arise when storage sites of remote memories are destroyed following widespread structural brain damage. Extensive remote memory loss has been observed in patients in whom evidence of significant cerebral pathology cannot be established (Kapur, 1994). It is thought to be a consequence of psychological distress and is often referred to as ‘psychogenic amnesia’. This term has been used to refer to discrete episodes of memory loss such as fugue states in which there is a sudden loss of autobiographical memory and personal identity, usually associated with a period of wandering. Fugue states usually resolve within a few hours or days although the patient may remain amnesic for the period in fugue. ‘Psychogenic amnesia’ has also been used to refer to persistent memory impairment in the absence of significant brain damage and in which the pattern of memory loss differs from that normally seen following organic brain damage. Neuropsychologists are frequently asked to give an opinion about the aetiology of cognitive and behavioural disorders, in particular, whether functional or organic factors account for impaired functioning. However, differentiation of organic and psychogenic amnesia can be difficult, particularly in patients in whom there is some evidence of organic brain damage in addition to psychological distress. Several criteria have been proposed to distinguish organic and psychogenic amnesia. However, the present paper presents a patient, JJ, who complains of profound retrograde amnesia following a mild head injury 3 years ago, but her clinical presentation does not conform to previous descriptions of organic or psychogenic amnesia. As a result, differential diagnosis proved difficult. CASE REPORT Reason for Referral JJ, a 56 year old right handed woman who had sustained a minor head injury at work in 1994, was referred by her general practitioner (GP) in December 1995 for a

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neuropsychological assessment as she was complaining of language and memory impairment. She was seen on four occasions during 1996. In February 1997, JJ’s solicitors contacted the Psychology Department to ask for a copy of the neuropsychological report to assist them with legal proceedings as JJ was pursuing a personal injury claim against her former employers. The author requested copies of all JJ’s medical and hospital records (including GP notes) which proved invaluable in aiding differential diagnosis. Whilst it is not uncommon for patients to be assessed by a wide range of professionals in different locations, it is unusual for clinicians to have relevant medical records from other hospitals made available to them during the course of routine health service work and GP notes are seldom available. JJ was re-assessed by the author in June 1997 and a separate report was prepared for legal purposes. History of Accident JJ had been injured at work on the 25th of August 1994 and sustained an injury to her left temple when someone opened a door as she was bending forwards. She did not lose consciousness but appeared dazed and complained of tingling in her arms and legs so she was taken to hospital. Her Glasgow Coma Score on admission was 15/15, indicating that she was fully conscious, but she appeared disorientated and amnesic for events following the accident. As a result she was admitted to hospital for observation, but discharged two days later when she no longer appeared disorientated. A male friend invited her to move into his bungalow after finding her sitting in a daze, complaining of shooting pains in her head, dizziness and a sense of depersonalisation a week after the accident in 1994. JJ was re-admitted on the 31st August 1994 as her confusion had increased and she was unable to recall recent events or even her name. In addition, she was noted to have an unsteady gait; her speech was slow, although articulated and coherent; and she continued to complain of numbness and tingling in her hands and feet. EEG and CT brain scan failed to detect any abnormalities. A Senior House Officer recorded in her medical notes that she had “unusual social circumstances” and an “odd affect”. She was discharged on the 2nd of September as she no longer seemed disorientated and she was able to remember the details of the accident. However, when reviewed at the ‘Head Injury’ Clinic thirteen days later, JJ complained of word-finding difficulties, excessive fatigue, dizziness and tingling in her arms and legs. She described her social situation to the Head Injury Coordinator who felt it may “be a major contributory factor to her problems following her head injury at work”. JJ had been living and working on the Continent, but had moved to England to live with her fiancé. When she arrived in the UK she discovered he was living with someone else. He suggested she live upstairs in his house whilst he lived downstairs with his new partner, so that he could give both women a trial and decide which one to marry. JJ subsequently ended the relationship and obtained work in a local café. She had only been there a short time when the accident happened. Review of Medical Notes The author did not have access to all of JJ’s medical notes until 1997 yet careful examination of handwritten clinical notes suggested functional factors may be of considerable significance in the aetiology of JJ’s amnesia. The notes indicated that JJ’s symptoms fluctuated considerably over time. The precise onset of her retrograde amnesia was difficult to determine but it is unclear whether this reflected symptom fluctuation or because remote memory loss is not routinely assessed in clinical practice. There was remarkable agreement between different medical professionals (Neurologists, Psychologists, Psychiatrists) that her physical and cognitive symptoms were unlikely to be due to organic factors alone and review of her GP records revealed that JJ had a significant psychiatric background. JJ was seen by a Consultant Neurologist in October 1994 who felt her symptoms were unlikely to be attributable to her minor head injury and referred her to a Neurosurgical Unit in London for further medical tests to determine whether she was suffering from some other underlying pathological condition. She was admitted to hospital for two weeks in

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December 1994 and assessed by Neurologists, a Clinical Neuropsychologist and a Psychiatrist. She complained of severe word-finding difficulties and memory impairment, but clinical notes indicated that she has been able to provide professionals with an account of the accident and events in her life leading up to the accident (although she remained unable to recall her stay in the local hospital immediately after the accident). JJ continued to complain of tingling in her arms and legs, but also intermittent headaches, numbness on the right hand side of her body and a feeling of “not being in her body”. Her speech was noted to be hesitant and stuttering and she exhibited naming and pronunciation difficulties. Again, her affect was described as being “odd”. She was orientated in time, place and person, but had difficulty retaining new information. Psychometric assessment revealed that she was functioning below average on verbal sub-tests from the Wechsler Adult Intelligence Scale (her poorest performance was on digit span) and she performed below expected levels on a verbal fluency test (please see Table II and page 8 for further discussion). However, the psychologist felt that the nature of her language disturbance was not consistent with dysphasia and concluded that non-organic factors were contributing to her difficulties. Neurological investigations (including EEG) were normal except for mildly raised protein in her CSF (0.9Gm/L) of doubtful significance and white matter changes of a nonspecific nature in the centrum semiovalae were noted on MRI brain scan (indicative of small vessel disease). These changes were noted to be minor and common in people of JJ’s age group, with a history of smoking. JJ’s physical and cognitive symptoms were considered to be incompatible with an organic aetiology. She was assessed by a psychiatrist who felt she was depressed and suggested her symptoms may serve some purpose in preventing her from facing her feelings about her ex-lover. She was prescribed anti-depressant medication prior to discharge and follow-up appointments were arranged at her local hospital. In March 1995 she was reviewed by the local Consultant Neurologist who noted that although her speech disturbance had improved, her memory appeared to have deteriorated as she was unable to tell him her name. He referred JJ to the neurosurgical unit again for further analysis of her “curious speech disturbance” and “bizarre and severe memory disorder”. She was no longer orientated in time and place, had difficulty recalling her age, date of birth, full address, the name of the current prime minister and she reported that on one occasion she had looked in the mirror and failed to recognise herself. Again, an organic basis for her symptoms could not be demonstrated. In April 1996 she complained of significant right-sided weakness during a follow-up appointment. The Consultant Neurologist noted that although she dragged the right leg a little when walking she was able to walk heel to toe. There was a reduction of all modalities of sensation on the right side and a non-organic disturbance of coordination in the right arm (she repeatedly hit the same point on her upper lip rather than her nose on the finger/nose test). Past Medical History JJ takes thyroxine replacement therapy following a partial thyroidectomy in 1980. Her thyroid function was found to be normal during the many neurological examinations she underwent. She had a hysterectomy in 1986. Psychiatric History JJ’s medical notes date back to 1957. She has a long history of depression and has taken psychotropic medication for many years. She was taking anti-depressant medication prior to the accident in 1994. References are made to episodes of depression in 1959 and 1968 for which she received electro-convulsive therapy (ECT), but no further information is available about these episodes. Thereafter there are frequent references to recurrent depression and anxiety for which JJ repeatedly received treatment from the Adult Mental Health Services. Comments made by different professionals who saw JJ over the years include: “She has been her usual self during this admission – histrionic, emotional, and inclined to be depressed. She is also a very kind person and well liked by both patients and staff”.

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“Her unhappy childhood has left her with a great feeling of insecurity and a tendency to make mountains out of molehills”. “She has been an unhappy, tense, anxious lady for whom it has only been possible to do a limited amount”. Correspondence in 1972 states that JJ had twins aged 12 years and a boy aged 4 years and was tense and anxious following the birth of an illegitimate child who was given up for adoption. She was married, but had left her husband on several occasions because he was violent towards her. The relationship ended in 1979. JJ married again in 1984, but this relationship ended in 1989. Letters sent to her GP following the accident in 1994 raise the possibility that JJ was abused during her childhood (it is not clear whether this was sexual or physical). She is described by friends as poorly educated and unable to manage on her own for any length of time. Descriptions of JJ’s behaviour over the years suggest longstanding difficulties. When this is considered in the context of an abusive and violent background it raises the possibility that JJ has a personality disorder (such as Dependent Personality Disorder), although this has never been formally diagnosed. Assessment in 1996 – Clinical Presentation JJ was cooperative during testing, but prone to outbursts of irritability and fatigue (at times she would close her eyes and appear to drift off). As a result, testing had to be carried out over three sessions in February and April 1996. She was accompanied by a male friend whom she shared a house with and a volunteer from ‘Headway’, a charitable organisation for people who have suffered a head injury. JJ complained of dizziness, headaches, fatigue, right-sided weakness, word-finding and single word comprehension difficulties, poor memory for recent events and remote memory loss. Although she was able to describe the accident she could tell the author very little about any other aspect of her life. For example: she was unable to name her parents or describe their appearance and she did not know whether she had any siblings; she was unable to recall where she went to school or what occupations she has had in the past; and she did not know whether she had ever been married or had children. She even claimed to be unsure of her identity. Her physical and cognitive symptoms were having a significant impact on her daily life and she required daily assistance from her house-mate and representatives from ‘Headway’ to cope with basic activities of daily living (e.g. cooking, finances, shopping, travel etc). JJ brought letters written by friends describing her premorbid personality and asked the author to read them. The letters described JJ as independent, helpful, caring, adaptable, easy-going and skilled at cookery, art, sewing, gardening and DIY, before the accident. Since the accident, JJ had become irritable, swears a great deal, displays inappropriate emotions and reports feeling emotionless at times. During the assessment, JJ exhibited unusual behaviour. For example, when frustrated by tasks involving concentration, she reported that she wanted to “blow out and smash” the author. At other times she would ask if her behaviour was considered ‘good’ or ‘bad’. Educational and Occupational Background The author was unable to obtain information from JJ about her educational and occupational background, but an informant told the author that JJ had lived and worked in hotels on the Continent during the previous five years. Her premorbid IQ was estimated to be in the average range for the following reasons: (1) Her highest scores on two sub-tests (picture completion and block design) from the WAIS-R, administered in 1994 were in the average range. (2) Her score on the Schonell reading test administered in 1996 was in the low average range, but this is likely to be an underestimate given her language problems.

NEUROPSYCHOLOGICAL TEST RESULTS

IN

1996

The results of neuropsychological testing are shown in Table I.

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Neuropsychological Test Results in 1996 General intellectual functioning Estimated premorbid IQ (Schonell) WAIS-R subtests age scaled Digit Span (F2B0) Vocabulary Similarities Picture completion Block design Digit symbol Prorated verbal IQ Prorated performance IQ

Language functioning

89

Graded Naming Test (McKenna and Warrington) Scaled score equivalent Verbal fluency (FAS) total Reading regular words (126) High frequency (42) Medium frequency (42) Low frequency (42) Reading exception words (126) High frequency (42) Medium frequency (42) Low frequency (42) Perception VOSP – Incomplete letters Executive functioning Verbal fluency Similarities

2 7 5 2 5 2 66 64

Anterograde memory Recognition memory test Words (50) 20 (< 5th percentile) Faces (50) 32 (< 5th percentile) WMS-R subtest scores Orientation (14) 2 (M 13.4, SD 0.6) Visual reproduction 1 (41) 5 (1st percentile) Visual reproduction 11 (41) 2 (1st percentile)

7 5 [25] 114 40 39 35 113 41 41 31 Pass 5 [25] 5

Remote memory Autobiographical memory interview Total score summary Section A: Childhood Section B: Early adult life Section C: Recent life Grand total

Personal semantic (max score + 21) *0 [< 11] *0 [< 14] *7 [< 17] *7 [< 47]

Autobiographical incidents (max score = 9) *0 [< 3] *0 [< 3] *2 [< 5] *2 [< 12]

Famous faces test

JM

Controls

Number of faces named Identifying information Total

6 16 22

31.1 + 9 ––– 39.3 + 8.8

Legend: (..) Total number of items in test. *Abnormal score. M and SD = mean and standard deviation scores obtained by standardisation sample […] cut-off scores. WAIS-R = Wechsler Adult Intelligence Scale – Revised; WMS-R = Wechsler Memory Scale – Revised.

Intellectual Functioning JJ was unable to complete the National Adult Reading Test so her premorbid IQ was estimated using the Schonell Reading Test and found to be in the low average range. Given her language impairment, this may be an underestimate of her true ability level. JJ’s current level of intellectual functioning was assessed using a shortened version of the Wechsler Adult Intelligence Scale-Revised and her prorated IQ was in the mentally retarded range. This may not be a reliable estimate of her current level of intellectual functioning because she was unable to complete many of the sub-tests from the Wechsler Adult Intelligence Scale-Revised, because of language, concentration/memory difficulties or fatigue. She completed five subtests; vocabulary, similarities, block design, digit span, picture completion and obtained

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low average, borderline, borderline, defective and defective scores respectively. Language JJ was given a 252 item reading task to assess her ability to read high, medium and low frequency regular and exception words (Patterson and Hodges, 1992). When reading single words, JJ had occasional difficulty translating orthography to phonology and would try to convey word meanings using circumlocutions e.g. “white stuff” for “snow”. She had equal difficulty reading exception and regular words, scoring 114/126 and 113/126 respectively. Control subjects make essentially no errors (1% or less) in reading regular words; and 5% errors on the low frequency exception words, but only 1% on medium and high frequency exception words. JJ’s reading score was abnormal, but not dramatically so. She was able to read nonwords, although her performance (23/40) on this test was below average (controls score an average of 39/40). Her scores on this test suggest she has mild phonological dyslexia, but the nature of her errors was not characteristic of this disorder. For example, she did not make semantic errors which are characteristic of deep dyslexia. Neither did she make phonemic errors or regularisations. Her spontaneous speech was characterised by word-finding difficulties and she obtained a low average score on a Graded Naming Test (6/30). Her performance on a verbal fluency test (FAS) was also very poor (5). She was unable to complete the Token Test of language comprehension because of memory and concentration difficulties. JJ was seen by a Speech and Language Therapist who noted that she presented initially with minimal word-finding difficulties and some non-fluency, but her symptoms worsened as the session progressed and she appeared to develop comprehension difficulties as well. When writing, JJ’s spelling was intact, sentences were usually grammatically correct, but she would occasionally omit personal pronouns (e.g. I), definite and indefinite articles (e.g. the, an) and conjunctives (e.g. and) which made text difficult to follow at times. Overall, her pattern of results on language tests did not conform to that seen in aphasic syndromes or reading disorders (dyslexias). This does not rule out the possibility that some of her difficulties are secondary to organic brain damage, but functional factors appeared to be operating. Executive Functioning JJ completed two tests of frontal lobe function (verbal fluency and WAIS-R similarities sub-test) and obtained scores in the borderline-defective range. She was unable to complete the Cognitive Estimates Test (Shallice and Evans, 1978) because of memory difficulties. When her performance on these tests is considered in the context of her personality change and unusual behaviour, it raises the possibility of frontal lobe dysfunction. Memory Anterograde Memory JJ’s anterograde memory was assessed using the Warrington Recognition Memory Test and subtests from the Wechsler Memory Scale-Revised. JJ was not

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orientated in time and place and her performance on a word and face recognition test was below the 5th percentile and worse than that seen in many neurological patients (her score was below chance on the word recognition subtest). Her performance on a test requiring her to memorise abstract designs (visual reproduction) was also impaired (1st percentile) and a test requiring her to recall a passage of prose (logical memory) was abandoned because of poor performance. Remote Memory JJ’s remote memory was assessed using two tasks designed to probe personal and public memory. The Autobiographical Memory Interview (Kopelman et al., 1989b) was used to assess personal semantic and episodic memory across three time periods: childhood, early adulthood and recent life. For each time period JJ was asked to give personal semantic information (e.g. location of secondary school) and autobiographical incident information (e.g. an incident which happened at school). JJ answered ‘don’t know’ to all questions concerning her childhood and early adulthood. She was able to provide a small amount of semantic information from recent life such as the name and location of the hospital in which this assessment was taking place and the name and location of the last hospital she had been admitted to. She could also state her home address. She was unable to provide any autobiographical incident information. Overall, JJ was significantly impaired in her ability to provide personal semantic and episodic information. JJ also completed an updated version of the Famous Faces Test described by Greene and Hodges (1996). It consists of 50 photographs of persons who were prominent for a limited time period between the 1940’s and 1980’s. There were ten photographs from each of the five decades including politicians, statesmen, stage, TV and film personalities and sportsmen. For each photograph there were two potential parts to the test; naming and identification. First JJ was asked to name the person in the photograph. Only a correct full name was accepted. If she was unable to name the person, she was asked to give some identifying information about them e.g. their occupation. Acceptable responses contained specific identifying information (e.g. Arthur Scargill was the leader of the miners) rather than vague statements (e.g. something to do with politics). JJ’s ability to name and provide basic identifying information about famous faces was significantly impaired. Phonemic and semantic cues did not assist her with this task. Her performance on this test was worse than that seen in patients with mild to moderate dementia. Comparison with Previous Psychometric Assessment Of particular note is the fact that JJ obtained satisfactory scores in 1994 on tests of non-verbal and visuo-perceptual skill, recognition memory tests, tests associated with executive functioning (Weigl Colour Form Sorting Test and Interpretation of Proverbs) and a test of object naming. Comparison of her performance on neuropsychological tests in 1994 and 1996 (see Table II) shows that in 1996 her performance on many tasks, most notably recognition memory

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TABLE II

A Comparison of Neuropsychological Test Results Obtained in 1994 and 1996 Tests General intellectual functioning Estimated premorbid IQ (schonell) WAIS-R subtests age scaled Digit Span Vocabulary Arithmetic Similarities Picture Completion Block Design Digit Symbol Prorated Verbal IQ Prorated Performance IQ Language Graded Naming (scaled score) Memory Recognition Test Words (50) Faces (50)

1994

1996

–––

89

3 (4F 2B) 6 7 8 9 11 ––– 75 –––

2 (2F 0B) 7 ––– 5 2 5 2 66 64

10

7

46 (50-75th percentile) 42 (25-50th percentile)

20 (< 5th percentile) 32 (< 5th percentile)

tests, but also naming and visuo-spatial skill tasks, was worse than that seen in 1994. The only possible organic explanation for this deterioration in performance is that JJ is suffering from a progressive neurological disease, yet there is no medical evidence which supports this hypothesis. NEUROPSYCHOLOGICAL TEST RESULTS

IN

1997

Research has shown that the ability of skilled clinicians to detect feigned neuropsychological deficits when provided with standard data from the WAIS-R and WMS-R seldom exceeds chance levels, but when tests of malingering are employed the detection rate significantly improves (Rogers, Harrel and Liff, 1993). The author re-assessed JJ in 1997 to administer tests of functional complaints and malingering and to examine the stability of her performance on certain tasks. JJ completed two tests designed to detect functional disorders or exaggeration of symptoms (Rey’s 15 items and Recognition versus Recall Memory: Lezak, 1995). Tests of malingering are based on the assumption that patients attempting to simulate a memory impairment are unlikely to be conversant with the true nature of amnesia and this will be apparent in the pattern of their performance. JJ’s performance on recall versus recognition memory tests was acceptable (i.e. recognition was better than recall), but her performance on Rey’s memorisation of 15 items was grossly abnormal. The principle underlying this test is that anyone who is not severely brain damaged or retarded can perform the test easily, but patients who wish to appear impaired often fail. After completing another memory test the author informed JJ that she had recalled a number of items correctly. JJ became very agitated and said ‘but it’s not true’ and insisted her answers were random guesses. Her performance on

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the Digit Span subtest from the WAIS-R was unchanged (DF2 DB2) from 1996. The author asked JJ for details of the accident in 1994 and the life events which preceded the accident, but JJ claimed she was unable to recall any of this information. She lost her temper when the author continued to question her, burst into tears and ended the interview. DISCUSSION This paper describes an unusual case of remote memory loss in a patient, JJ, who shows no evidence of significant structural brain damage. Her clinical profile does not fit with previous descriptions of either organic or psychogenic amnesia making differential diagnosis difficult. Differentiating organic and functional complaints relies on the context and circumstances of the presenting problems as well as clinical and neuropsychological features. Criteria have been proposed to help clinicians distinguish organic and functional complaints. However, the present case and recent reports in the literature of patients who present with remote memory loss following mild head injury, suggest the usefulness of current diagnostic criteria may be limited. Points in Favour of an Organic Hypothesis Factors which suggest an organic aetiology include the following (Lezak, 1995); (1) cognitive impairment appears during or after illness, intoxication, head trauma or severe malnutrition etc, (2) the patient exhibits neurological symptoms (e.g. hemiplegia) in addition to cognitive impairment, (3) the pattern of cognitive impairment is similar to that seen in other patients with organic conditions and symptoms make medical sense, (4) the pattern of cognitive impairment involves lateralized abilities, (5) the pattern of memory impairment is such that recent memory is more severely affected than remote memory, (6) remote memory loss, if present, is temporally graded and does not involve loss of personal identity, (7) recovery of function is partial rather than complete, (8) the patient does not have a significant psychiatric background and has not been exposed to stressful life events in the months preceding the onset of cognitive impairment, and (9) there is no evidence of secondary gain. JJ’s amnesia was preceded by a mild head injury. There is nothing in her history to suggest her difficulties are congenital. JJ was unable to provide a detailed educational and occupational history, but she has had extensive contact with services throughout her life and there is no mention of cognitive impairment prior to her accident. Psychometric assessment shortly after the accident found her to be functioning in the average to low average range on many tests. Her performance has deteriorated since then, raising the possibility that she is has a progressive neurological disease. Indeed, she presents with symptoms indicative of organic brain damage such as dizziness, tingling in her limbs, right-sided weakness, generalised intellectual decline, language impairment, significant anterograde amnesia and personality/behavioural change. MRI scan found evidence of small vessel disease. However, all of the

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neurologists who have seen JJ insist that the minor abnormalities detected on brain scan can not account for the severity of her cognitive impairment. These abnormalities are often seen in patients of her age with a history of smoking, and in patients who do not show evidence of significant cognitive impairment. Her CSF protein levels were mildly elevated (0.9Gm/L), but again, this is not thought to be of any great significance. Other factors which might be taken as evidence that organic pathology underlies JJ’s difficulties include the following: (1) Global cognitive impairment, as shown by JJ, is rarely seen in cases of psychogenic amnesia. Usually, these patients exhibit severe deficits in remembering autobiographical material, whilst semantic knowledge, anterograde and procedural memory remain intact (Markowitsch, 1996), though this is not always the case (Papagno, 1998; De Renzi, Lucchelli, Muggia et al., 1997); (2) There has been no recovery of JJ’s remote memory loss which suggests an organic aetiology, although there have been reports in the literature of recovery from retrograde amnesia in patients with presumed organic amnesia (Papagno, 1998; Lucchelli, Muggia and Spinnler, 1995). Points in Favour of a Functional Hypothesis Factors which suggest a functional aetiology include the following (Lezak, 1995); (1) the onset of cognitive impairment is preceded by emotional stress, (2) the patient is emotionally distressed and/or has a psychiatric background, (3) there is evidence of secondary gain, (4) organic pathology which might account for the level of cognitive impairment cannot be demonstrated, (5) symptoms exceed what an injury/illness would be expected to cause, (6) the patient’s behaviour during testing is unusual in some way e.g. they give ‘don’t know’ responses to many questions, they exhibit ‘la belle indifference’, (7) the patients performance is inconsistent both between tasks and over time, (8) scores fall below chance level, and (9) an organic pattern of memory impairment is not evident. JJ had been dealing with a stressful life event just before the onset of her cognitive impairment and review of her GP records revealed an extensive psychiatric background which suggests she may be particularly vulnerable to stress. The pattern and severity of JJ’s cognitive impairment is at odds with the minor nature of her head injury and performance on neuropsychological tests has been inconsistent, below chance on occasion; and there was an inexplicable deterioration in JJ’s performance on psychometric tests between 1994 and 1996. Review of hospital records (particularly hand written clinical notes) indicates that the extent of her remote memory loss may have fluctuated over time, although it is difficult to date the precise onset and extent of her retrograde amnesia as remote memory is not routinely assessed in clinical practice. The extent of JJ’s retrograde amnesia covers her entire life span, yet remote memory loss is usually temporally graded and post encephalitic patients, who often show significant retrograde amnesia, rarely exhibit an amnesia which covers the entire life span (De Renzi and Lucchelli, 1993). JJ’s autobiographical deficit was paralleled by an equally severe amnesia for famous faces, yet many of the

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organic amnesia cases reported in the literature exhibit material specific deficits (Levine, Black, Cabeza et al., 1998; Mackenzie Ross and Hodges, 1997; Kroll, Markowitsch, Knight et al., 1997; Evans, Breen, Antoun et al., 1996; Stracciari, Ghidoni, Poletti et al., 1994; Hodges and McCarthy, 1993; Markowitsch, Calabrese, Liess et al., 1993; Kapur, Ellison, Smith et al., 1992; Tulving, Schacter, McLachlan et al., 1988). Neuropathological studies suggest that damage to the left temporal lobe of the brain is associated with loss of semantic knowledge, whilst right temporal lobe damage is associated with autobiographical memory loss (Kopelman, 1997). Extensive bilateral damage is thought to underlie ungraded retrograde amnesia, yet JJ does not show evidence of diffuse brain damage to account for her ungraded amnesia. These factors suggest that JJ’s amnesia may be functional rather than organic, particularly in view of the fact that she also exhibits many of the criteria identified by Kopelman (1997) as predisposing individuals to developing psychogenic amnesia. For example, patients with psychogenic amnesia often have a history of transient organic amnesia which may act as a learning experience. JJ received ECT in the past and is likely to have experienced transient amnesia and she sustained a minor head injury in 1994 resulting in a period of confusion and disorientation. Severe stress such as marital discord, bereavement, financial problems, offending behaviour or stress during wartime, usually precedes the onset of psychogenic amnesia. JJ had given up her job and home on the Continent to move to the UK and marry her fiancé, but he was having a relationship with another woman. Depression is common prior to the onset of psychogenic amnesia and JJ was taking anti-depressant medication prior to the accident in 1994. To summarise, there are a number of factors which suggest psychological processes are involved in the aetiology of JJ’s amnesia. The next issue is to identify the nature of her amnesia and whether it is simulated or unconscious. Psychogenic Amnesia Two types of psychogenic amnesia have been identified. Temporary fugue states and persistent remote memory loss in the absence of cerebral pathology. The underlying mechanisms which might account for psychogenic amnesia could be unconscious (hysteria) or conscious (malingering). Malingering can be suspected when there is evidence of secondary gain (such as escape from an unpleasant situation or compensation). One possibility is that JJ is simulating her amnesia for secondary gain. Indeed, she is receiving a considerable amount of practical and emotional support as a result of her amnesia and she is now involved in litigation. Subtle fluctuations in her symptoms over time may be interpreted by clinicians as evidence of malingering. On the other hand, as far as friends and family are concerned she has maintained her presentation for a prolonged period of time which suggests other psychological processes may be involved in the aetiology of her amnesia. For the time being, let us assume she is not simulating her amnesia and compare her with other cases of psychogenic amnesia reported in the literature.

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Fugue States Fugue states are characterised by an abrupt loss of personal autobiographic memory and personal identity associated with a period of wandering. Anterograde amnesia is not present and the remote memory loss usually resolves in a matter of hours or days (although the person usually has an amnesic gap for the period in fugue). JJ’s amnesia was identified after a series of hospital visits rather than a period of wandering, but her claim to be unsure of her identity might be considered by many clinicians to be a hallmark of psychogenic amnesia. However, the prolonged duration of her amnesia sets her apart from the majority of fugue states reported in the literature (except in the case reported by Kopelman, Christensen, Puffett et al., 1994, where malingering was suspected); as does the fact that she shows evidence of widespread cognitive impairment which is not usually associated with fugue states. Psychogenic Amnesia – Prolonged A small number of patients with prolonged retrograde amnesia following brain injury or disease, but in whom evidence of structural brain damage cannot be found, have been described in the literature (Barbarotto, Laiacona and Cocchini, 1996; De Renzi, Lucchelli, Muggia et al., 1995; Stracciari et al., 1994; Lucchelli et al., 1995; Starkstein, Sabe and Dorrego, 1997; Papagno, 1998; De Renzi et al., 1997). Comparisons will be made between JJ and other cases of remote memory loss following head injury. Review of the literature indicates the following features are common in cases of prolonged retrograde amnesia following head injury: (1) Patients frequently present with a dense retrograde amnesia covering their entire life span with little evidence of a temporal gradient (De Renzi et al., 1997; Papagno, 1998; Barbarotto et al., 1996; De Renzi et al., 1995; Lucchelli et al., 1995; Starkstein et al., 1997). The exception to this are the two cases reported by Stracciari et al. (1994) in which remote memory loss was confined to a period of 1 year and 10 months respectively. (2) Patients frequently present with loss of personal identity and a failure to recognise close friends, relatives or familiar places (De Renzi et al., 1997; Papagno, 1998; Barbarotto et al., 1996; De Renzi et al., 1995; Stracciari et al., 1994; Lucchelli et al., 1995; Starkstein et al., 1997); factors which are usually considered to be characteristic of fugue states. (3) In about half of these cases, remote memory loss has encompassed both personal and public information (Barbarotto et al., 1996; De Renzi et al., 1995; Lucchelli et al., 1995; De Renzi et al., 1997; Papagno, 1998). (4) Generalised intellectual and/or language impairment and other types of memory impairment, such as anterograde amnesia or semantic memory loss are rare. As a result, patients are often able to re-learn autobiographical information, though it may lack a sense of familiarity. (5) Structural brain imaging does not reveal evidence of cerebral pathology, but abnormalities may be detected by EEG or functional brain scans (Stracciari et al.,

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1994; Papagno, 1998; Lucchelli et al., 1995; Starkstein et al., 1997). A significant psychiatric history or evidence of secondary gain which might otherwise account for a patient’s presentation cannot be identified. Thus, the aetiology of remote memory loss in these cases remains a mystery. JJ presented with a dense retrograde amnesia involving personal identity, autobiographical and public facts. Structural brain imaging failed to detect any significant abnormalities (unfortunately, permission for a functional brain scan could not be attained). However, JJ is not typical of previously reported cases because she shows evidence of widespread cognitive impairment and she has a significant psychiatric background. Whilst there have been two previous reports in the literature of cases of remote memory loss following head injury in which the patient shows evidence of additional cognitive deficits, neither case has a significant psychiatric background. Patient CL reported by Papagno (1998) showed evidence of impaired verbal fluency and material specific naming deficits in addition to remote memory loss, whilst new learning was intact. However, unlike JJ, CL’s remote memory loss recovered progressively after about 10 days as his ability to relearn autobiographical facts led to the development of clear recollections. JJ has more in common with De Renzi et al.’s (1997) patient ‘Andrea’ who showed evidence of widespread cognitive impairment in addition to remote memory loss. Like JJ, Andrea exhibited semantic memory loss, single word comprehension deficits, impaired verbal fluency, reading and writing deficits and impaired ability to perform well learned motor activities such as shaving. New learning was preserved which allowed Andrea to re-learn autobiographical information although a sense of familiarity was lacking. De Renzi et al. (1997) advocate the creation of a third nosographic entity to define patients who show a lasting loss of remote memory after a minor head injury in the absence of recognisable organic or psychological factors which could account for their deficits. However, JJ does not fit into this category because unlike the other cases reported in the literature she does have an extensive psychiatric background. It is possible that, in many of the previously reported cases, psychological factors were crucial in the aetiology of amnesia, but were not detected during assessment (Kopelman, 2000) or were dismissed as unimportant by the authors. For example, six months prior to the onset of CL’s amnesia (Papagno, 1998), his girlfriend broke off their relationship leaving him very depressed. He attempted to meet with her repeatedly, whilst she avoided him. On one occasion he left home suddenly and telephoned his girlfriend to say he was sleeping on the road. When he returned, he threatened to kill his girlfriend and was suicidal. CL had stopped speaking about his girlfriend one month prior to the accident and was thought to have accepted the situation. De Renzi’s patient, Andrea, was having difficulty obtaining payment for building work he had carried out in the 6 months preceding his accident. Although he was described as ’not manifesting any major signs of anxiety’ he was suffering from insomnia. With regard to equivocal cases, two things can be learned from review of the literature: (1) when investigating patient’s psychological background, reliance should not be placed on patient or carers reports. Independent investigations should be carried out in addition. For example, JJ did not admit to any social or psychological problems whatsoever and it took a large number of telephone calls, interviews with friends/carers, review of medical records (which were only made

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available to the author because of ongoing litigation), to discover that JJ had an extensive psychiatric background; (2) When background psychological factors are detected, a detailed account of the psychological and social context should be provided so that the reader can evaluate their significance (Kopelman, 2000). When there is no evidence of significant structural brain damage, differentiating between psychogenic and organic retrograde amnesia is difficult, yet it is important to do so because it has implications for treatment. In cases of presumed psychogenic amnesia patients may share features associated with organic amnesia and vice versa. For example, loss of personal identity and rapid recovery of function have been considered hallmarks of psychogenic amnesia yet both have been reported in cases of presumed organic amnesia (Lucchelli et al., 1995). Loss of personal identity has been absent in cases of presumed psychogenic amnesia (Barbarotto et al., 1996) and the presence of a temporal gradient has been absent in some cases of presumed organic amnesia (Lucchelli et al., 1995). Differential diagnosis is most difficult in cases, like JJ, where there may be an interaction between the effects of a brain lesion and a patient’s emotional predisposition. It is often assumed that amnesia is either organic or psychogenic, yet there may be an interaction between these phenomena. There could be an underlying vascular basis for some of JJ’s difficulties, but there appears to be considerable non-organic elaboration. JJ has been disabled by neurotic problems for most of her life and neither the minor head injury she sustained, nor the small vessel disease observed on brain scan, can be the cause of all of her difficulties. The failure to find evidence of cerebral pathology does not rule out the possibility that organic factors are involved in the aetiology of a disorder; and the presence of a neurological abnormality does not rule out the possibility that psychological factors are also operating. Review of the literature suggests that in some cases retrograde amnesia may be a result of the destruction of engrams (Mackenzie Ross and Hodges, 1997), but in other cases, like JJ and previously reported cases of remote memory loss in the absence of significant structural brain damage, retrograde amnesia may be attributable to other factors, such as a retrieval deficit. Certainly, reports of recovery of function following exposure to environmental cues, hypnosis and amytal injection suggest a retrieval deficit underlies many instances of remote memory loss. Markowitsch (1996) proposes that organic and psychogenic amnesia are comparable and that similar underlying brain processes account for these deficits. These processes affect access to stored engrams. Prefrontal brain damage has been associated with retrieval deficits (Della Sala, Laiacona, Spinnler et al., 1993) and interestingly, JJ shows signs of frontal lobe dysfunction. However, other psychological processes such as repression and dissociation have also been suggested as potential explanatory mechanisms for remote memory loss, as has motivated forgetting such as malingering. Thus retrieval deficits can be secondary to organic brain damage or conscious/unconscious psychological processes. It seems likely that both organic and psychological factors are involved in the aetiology of JJ’s amnesia, the latter to a much greater degree. Perhaps an initial period of true amnesia has been replaced by a functional amnesia; or a genuine amnesia (e.g. secondary to frontal lobe dysfunction) has become exaggerated for secondary gain. JJ’s clinical history suggests she may

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have a Dependent Personality Disorder and her amnesia may serve to retain the attention and care other people have demonstrated since her head injury. In conclusion, JJ’s clinical profile does not fit with previous descriptions of organic or psychogenic amnesia making differential diagnosis difficult. She has much in common with a number of other cases reported in the literature of prolonged remote memory loss following mild head injury which do not fit the diagnostic criteria for organic or psychogenic amnesia either. Thus, JJ lends support for De Renzi’s call for a third nosographic entity to define these patients. However, unlike previously reported cases, JJ has an extensive psychiatric history and there is reason to believe she may have a Personality Disorder. Her amnesia may have been triggered initially by organic factors but appears to have become exaggerated over time. Unfortunately, it is not possible to determine the extent to which unconscious (hysteria) or conscious (malingering) factors underlie her disorder. Further research is needed to examine the structure and organisation of remote memory and how it breaks down following brain damage or emotional trauma. Measures should be developed which will allow researchers to identify and explore the nature of retrieval deficits and studies should be complemented by functional as well as structural brain imaging. Acknowledgements. The author wishes to thank the following people for their helpful comments on this paper: Professor Michael Kopelman, Professor Peter Fonagy, Dr Anthony Roth, Dr Peter Scragg, Dr Janet Feigenbaum and Mr Stephen Dunevein.

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(Received 4 March 1999; accepted 13 March 2000)