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Reduplicative Paramnesia: A Disconnection Syndrome of Memory
REDUPLICATIVE PARAMNESIA: A DISCONNECTION SYNDROME OF MEMORYl R. Dennis Staton, Roger A. Brumback and Helen Wilson (Psychiatry Service and Neurology Service. Veterans Administration Medical Center and UND School of Medicine. Fargo. North Dakota. and Department of Psychology. Moorhead State University. Moorhead. Minnesota)
INTRODUCTION
The Capgras syndrome (Capgras and Reboul-L'achaux, 1923) is characterized by failure to recognize a familiar person (or persons), associated with belief that the real person has been replaced by a double. This syndrome is a variant of the phenomenon of reduplicative paramnesia (Pick, 1903), which may include duplication (called reduplication by Pick) not only of familiar people but also of self, of places, and of time and events (Abrams, 1977; Alexander, Stuss and Benson, 1979; Weinstein, 1969). Even though Capgras symptoms have typically been attributed to functional psychosis. a variety of organic brain lesions have been shown to produce duplication syndromes (Alexander et al., 1979; Weinstein, 1969; Weston and Whitlock. 1971; MacCallum, 1973; Benson, Gardner and Meadows, 1976; Merrin and Silberfarb. 1976; Hayman and Abrams. 1()77; Christodoulou. 1()7H; Nikolovski and Fernandez, 1978). Although Pick used the term paramnesia to indicate that the duplication symptoms were related to a disturbance of memory, recent authors have focused upon visual perceptual problems, including prosopagnosia (Alexander et al., 1979; Benson et al.. 1976; Hayman and Abrams, 1977; Granacher. 1978; Shraberg and WeitzeL 1979). and/or frontal lobe apathy (Alexander et al., 1979; Benson et al., 1976) as an explanation of duplication syndromes. We agree with Pick, that the central pathology of these syndromes is a disturbance of memory. We describe a case of post-traumatic reduplicative paramnesia in which the symptoms appear to derive from impairment of integration of newly acquired information with older memories. lPresented in part at the Second European Conference of the International Neuropsychology Society, Noordwijkerhout. Holland. June 30. 1979. Cortex (1982) 18, 23-36.
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R. Dennis Staton, Roger A. Brumback and Helen Wilson
CASE REpORT
The patient, RK, with no prior history of psychiatric or neurologic impairment. was found unconscious on July 25, 1970, at age 23 years, after a single-car accident. On admission to the hospital, x-ray studies revealed no skull fracture. He remained comatose for seven days, but then made a rapid recovery and was discharged on the 25th hospital day. Repeat neurologic examinations during the years following his accident have shown very slight left hyper-reflexia, left extensor plantar response (Babinski reflex), and a mild left central facial nerve palsy. Gait unsteadiness present for several months after the accident has resolved. Visual fields are normal. Three electroencephalograms done since the accident have demonstrated right te~poral slowing. Four-vessel cerebral angiography performed eight years after the aCCident showed no abnormality. The results of computerized axial tomographic (C AT) scanning also done eight years post-accident are described below. Two months after the accident the patient was referred for neurosurgical evaluation of left hand "numbness" (now resolved) and a change in personality. At that time, his parents reported that approximately five weeks after the accident RK developed new and uncharacteristic behaviors. He became persistently irritable and angry, with temper outbursts and an uncooperative and belligerent attitude. Examination at that time revealed retrograde amnesia and difficulty learning new information . With the exception of these reported impairments of personality and memory, and a very slight gait impairment, RK was considered by his neurosurgeon to have made an excellent recovery from his head injury. Two years after the accident the patient unsuccessfully attended business college, attributing his failure to difficulty with memory. In the first months after his accident, RK experienced feelings of "unreality" . These feelings persisted, but were not reported by RK to his physician until 1974, four years after his accident, when he was hospitalized because of his explosive temper. His parents reported then that RK had developed additional problems of feeling victimized, blaming others, and social withdrawal. These factors, along with his persisting poor frustration tolerance and impulse control, had contributed to numerous employment failures and repeated conflicts with his family. During the 1974 hospitalization, RK described a conviction that all of his current experiences had happened before . His condition was described as deja vu by psychiatric and psychologic consultants, who considered his emotional problems " psychogenic" in origin. On referral to us in October 1978, eight years after his accident, RK was age 31, unmarried and unemployed. He felt desperate and described living in a world that ' seemed to be a fantasy. He stated that "everything is so different" (than before the accident). Friends .and relatives, including his parents and siblings, were not "real" - but were slightly different " look-alikes", or doubles - not the real people he had known before the accident . This was also true of places, including the family farm and the city where he was hospitalized. "They didn't have this kind of hospital in Fargo . I must be somewhere else." He did not know where he was. He didn't know where his true relatives were, but he was sure that the present "relatives" were false duplicates. He recognized them as duplicates through differences between their current behavior (or appearance) and his recollections from the past. "This person cannot be my cousin because my real cousin worked at a different job." The family farm was a false duplicate because recently added buildings "don't seem as if they should have been built." His cat was not real because of a new scar on one ear. He even denied that he could be the true RK because several aspects of his present appearance (including a lost tooth and a foot callus) were different than he remem-
Reduplicative paramnesia
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bered. "If I were really me I'd have a place of my own. I'd be working." In spite of being able to recount evidence to the contrary, he believed that he had not actually lived in a certain city for two years after the accident. "I would never do that!" He referred to his parents as "those people". His father could not be real because "he has tractors that my (real) father wouldn't have bought." "He wouldn't have expanded the milk business." The unreal people, places, objects, and experiences were not perceived as exact duplicates. They were all slightly different from past appearance or recollection. These differences between his present observations and his past memory provided the evidence for duplication. He stated that "the problem is that my memory is too good. " He had no difficulty identifying objects. RK described several elaborate delusions (or confabulations) which eased the desperation of his "unreal" life. He believed that the entire eight-year period of disability and "unreality" lived since the accident had really occurred some time previously and had culminated in complete recovery. He expected his current reliving of past life experiences, although entirely unreal, to have the same optimistic outcome (that is, he would recover). It was in this context that all current experiences seemed to be false duplications of similar previous experiences. RK also believed that the present time could not be October 1978. It was "approximately 1975", because: (1) his physician had told him that he would be "nearly back to normal", married, and working by the time he was age 30 (which would be the year 1977); and (2) his old girlfriend, who had recently married someone else, would still be single if it were 1975. Consistent with this disorientation to time, he denied the reality of recent world events. RK stated that "I can't trust anything." "I don't have control over things that are happening to me." Although RK was very suspicious, he had no paranoid conviction of a plot against him. A moderately severe reactive depression was present. manifested by depressed affect, low self-esteem, pessimism regarding the future, and a feeling that he might be better off dead. There was no evidence suggesting the presence of a delusional endogenous depression, schizophrenia, drug toxicity, or exceptional situational stress. We considered RK to be psychotic, in that he maintained irrational beliefs, and we attributed this psychosis to his structural brain injury. RK had been medicated at different times during the preceding four years with the dopamine-blocking agents trifluoperazine 2 mg t.i.d. and haloperidol 1 mg t.i.d .. without benefit. In spite of these failures. we decided to assess the possibility of a dopaminergic basis to RK's psychosis with a 23-day trial of combination carbidopa/L-dopa 25 mg /250 mg tablets, with doses increasing to a maximum of 8 tablets per day. On this regimen he showed progressively worsening symptomatology, and after three days on the maximal dosage he reported that: "Things are even more unreal. I feel totally out of place. There isn't any such place as this. I don't believe this. I don't believe this is a real hospital." The carbidopa/L-dopa was stopped and RK was subsequently given fluphenazine hydrochloride. He showed marked symptomatic improvement four days after the dosage of fluphenazine hydrochloride had reached 12.5 mg per day. Both his duplication experiences and his SUbjective distress were lessened. His family members were now perceived as real. He explained his previous inability to recognize family members by stating: "I remember them differently." He remained slightly troubled by some behaviors of family members, feeling that they were doing things that they "shouldn't be doing" (according to his past memory of them). His disorientation for time also persisted.
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R . Dennis Staton, Roger A. Brumback and Helen Wilson
CAT SCAN RESULTS
CAT scanning performed November L 1978, revealed the following lesions (Figure 1): (1) atrophy in the region of the posterior right hippocampus and adjacent temporal lobe. (2) a discrete area of moderate atrophy deep in the posterior-superior temporal lobe at the temporo-parietal junction, in a region traversed by occipito-temporal fibers, (3) mild atrophy at the right parieto-occipital junction, (4) mild peri-Sylvian atrophy of the right posterior frontal operCUlum, and (5) mild, diffuse frontal lobe atrophy. NEUROPSYCHOLOGICAL Ev ALUATION
Behavioral Observations RK appeared at the appointed time for the current test battery, but expressed ambivalence about the procedure. He was suspicious, questioning each test and the consequences of responding. His experiences following the accident were related with a bland lack of concern during the evaluation interview. Despite apparent hostility, he completed all tasks and seemed motivated to perform well. At the time of this neuropsychological evaluation , RK was receiving no medication.
Fig. I - CA T scan sections showing atrophy in the region of the posterior right hippocampus and adjacent temporal lobe, and atrophy in the right posterior-superior temporal lobe at the temporo-parietal junction.
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27
Intelligence Testing Wechsler Adult Intelligence Scale (WAIS) testing conducted 2 months after RK's accident and repeated 8 years later showed Verbal IQs of 93/106, Performance IQs .of 72/95, and Full Scale IQs of 83/102. Improvement occurred in overall intellectual capability, particularly in nonverbal skills, although a mild Verbal-Performance discrepancy remained. This persistent Performance IQ deficit suggests a right hemisphere disturbance involving primarily nonverbal cognitive functions, with the relatively lower scores on Digit Symbol, Block Design, and Object Assembly sub tests (on current testing) suggesting the presence of visual perceptive impairment.
Memory Testing Memory was tested using the Wechsler Memory Scale (WMS), the Graham-Kendall Memory-For-Designs, and the Benton Visual Retention Test. RK's Memory Quotient was 90. His poor performance on the Logical Memory sub test of the WMS suggested mild concentration, integration, and/or retrieval deficit. The most significant deficiencies were found in short term visual memory and reproduction of designs.
Neuropsychological Battery RK showed mild to moderate impairments in nonverbal abstraction and problem-solving (Category Test), nonverbal auditory perception (Rhythm Test), tactual memory and motor problem solving (when using his left hand) on the Tactual Performance Test (TPT). Right hand performance on the TPT was normal. There was no evidence for a language disturbance on the Halstead-Reitan Aphasia Screening Test. There was some indication of a mild constructional apraxia in a task which involved copying a Greek cross. Speech perception was normal. These results provide supporting evidence of dysfunction in the right hemisphere, with primarily temporal lobe localization. The patient also showed deficient performance on the following tests: Porteus Mazes (performance deficits in ordering, planning, and foresight), Trails A and B (deficient visual sequencing and. motor speed), and the Finger Agnosia and Fingertip Writing subtests (impaired tactile preception) ..These results did not suggest lateralized dysfunction.
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R. Dennis Staton, Roger A. Bmmback and Helen Wilson
Motor Tests All tests of motor skills, including finger tapping and grip strength, were in the normal to above average range.
Summary of Neuropsychological Testing Neuropsychological deficiencies were found in the following tests: Dysfunction
Test Revealing Deficit
1. Visuospatial (visual perceptive) skills
W AIS Performance Scale subtests Copying Greek cross
2. Visual memory and reproduction
Visual Reproduction subtest of the WMS Benton Visual Retention Graham-Kendall Memory-ForDesigns Seashore Rhythm Perception Test
3. Nonverbal auditory perception 4. Problem solving
Halstead Category Test Tactual Performance Test (TPT) Porteus Mazes (Vineland Revision)
This overall pattern of neuropsychological deficit is consistent with right hemisphere dysfunction, primarily of the posterior association cortex (Milner, 1958; Russell, Neuringer and Goldstein, 1970; Lezak, 1976). RK demonstrated difficulties with nonverbal auditory discrimination, a perceptual disorder associated with posterior right temporal lobe dysfunction (Milner, 1962), but did not show amusia, which is related to more anterior temporal lobe lesions. The TPT (particularly the memory component) relies heavily on nonverbal learning, which is considered a right hemispheric function. Teuber and Weinstein (1954) have shown that posterior right temporo-parietallesions (near the temporo-occipital boundary) may result in impaired performance on the TPT. Precentral (motor strip) frontal lobe damage can also impair TPT performance (Reitan, 1964), but such damage was not suggested by our motor testing. The deficits found on the Category Test (a measure of nonverbal abstraction) may be localized to the right temporal and/or frontal lobes. Involvement of occipital lobe function is suggested by impaired visual memory and perception. Since no primary visual deficit was evident in this patient, his occipital impairment seems to result from interruption of visual input to the temporal lobe. Thus, the functional deficits observed in this
Reduplicative paramnesia
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patient are primarily in the right temporal lobe. Minor right parietal and fro n t'al lobe involvement is also suggested.
Personality Testing RK's parents have reported in clinical interviews since the accident that their son has manifested the following new traits: feeling victimized and blaming others, emotional irritability, anger, social withdrawal, dependence, and apathy. A behavior questionnaire developed by Bear and Fedio (1977), used to assess disturbances presumably related to limbic system dysfunction, was administered to our patient. On this questionnaire, as on the Minnesota Multiphasic Personality Inventory (MMPI), RK denied most abnormalities. A separate Bear-Fedio rater form was completed by the parents, who perceived RK as suspicious, angry, easily frustrated, emotional, aggressive, depressed, and repetitive in his thinking. MMPI and projective drawing tests were administered to RK at the time of neuropsychological evaluation. Interpretation of RK's MMPI profile is complicated by marked elevations on the validity scales. The F-K index (-16), along with the high L Scale (= 70), strongly suggests excessive denial of emotional problems and an intense need to present a good image. The profile configuration showed elevations on Scales 4 and 8 indicating general social maladjustment. Personality traits compatible with the 4-~ configuration and found in RK include immaturity, low self-esteem, feeling victimized and blaming others, anger, suspiciousness, feelings of alienation, and social isolation. Testing also revealed authority conflicts and complaints against family. The most striking findings in RK's MMPI data and his projective tests are: (1) a high degree of suspiciousness, (2) a guarded approach to social relationships, (3) marked isolation and constricted expression of emotions, and (4) a sense of unreality about himself and the world. Repeat MMPI testing after six months of therapy with fluphenazine hydrochloride revealed a reduction in the intensity of these traits, with Scales 4 and 8 reduced to within the normal range. DISCUSSION
The patient described in this report has reduplicative paramnesia (Pick 1903), including Capgras symptoms (Capgras and Reboul-L'achaux, 1923). Weinstein has reviewed the phenomenon of reduplication, which may include duplication of time and events, of place, of person, of self, of body parts (usually the non-dominant upper extremity), and of objects (Weinstein, 1969). Such duplications result from brain injury of various causes (Alexanderet al., 1979; Weinstein, 1969; Weston and Whitlock, 1971;
30
R. Dennis Staton, Roger A. Brumback and Helen Wilson
MacCallum, IY73;Bensonetal., IY76;MerrinandSilberfarb, 1976; Hayman and Abrams, 1977; Christodoulou, 1978; Nikolovski and Fernandez, 1978). Our patient suffered closed head trauma and subsequently manifested duplications of place, of person (including self), of time and events, and of certain objects. Patients with reduplicative paramnesia frequently explain their duplication(s) with confabulation: an irrational explanation occurring in the presence of memory dysfunction (Weinstein, 1969). Our patient's delusional explanation that his current predicament derives from his living in a "fantasy world" (described in the case report) represents such a confabulation. Reduplicative paramnesia may bear a relationship to primary amnesia. Angelergues (1969) defines two basic aspects of primary amnesia. One aspect is Korsakoff's syndrome, resulting from lesions of diencephalic areas or the memory circuit 2 , or, less commonly, from lesions of the occipital cortex. Angelergues considers Korsakoff's syndrome to include three elements, all of which are demonstrable in our patient: (1) disorientation, (2) confabulation, and (3) amnesia in the special sense of inability to integrate present and past memories. Our patient's disorientation is manifested by failure to recognize family members, certain places, and present time as real. His explanation of the duplications is confabulatory, as previously described. Like the patients reported by Alexander et ai. (1979) and Benson et ai. (1 Y76), our patient is able to register new information, but fails to integrate. this new memory with past memory. While we do not equate reduplicative paramnesia with Korsakoff's syndrome, the reduplication phenomenon does appear to satisfy criteria for inclusion as a primary amnesia analogous to Korsakoff's syndrome. Thus, patients with both reduplicative paramnesia and Korsakoff's syndrome are disoriented, frequently confabulate, and experience difficulty comparing and integrating present cues with past experience (see Table I). The striking difference between these disorders is that with reduplicative paramnesia the patient is aware of contradictions (related to the duplication), while such awareness is absent in Korsakoff's syndrome (Grunthal, 1947). The second basic aspect of primary amnesia defined by Angelergues (1969) is amnesia of registration of new information, resulting primarily from hippocampal lesions (Scoville and Milner, 1957; Penfield and Milner, 1958; Milner, 1965; Milner, 1968; Penfield and Mathieson, 1974). Our patient shows impaired registration of visuospatial memory (perhaps explained by the posterior hippocampal atrophy demonstrable by CAT scan). Similar visuospatial impairment, along with frontal lobe impairment, was noted in the patient reported by Alexander et al. (1979), and these authors attributed 2The memory circuit described by Angelergues (1969) includes Ammons horn, fornix. hypothalamus. mammillary bodies, bundle of Vicq d'Azyr, anterior thalamic nuclei, and cingulum.
Reduplicative paramnesia
31
their patient's persisting duplication of place to the frontal lobe damage . Although our finding of minor frontal lobe atrophy by CAT scan (and midly impaired abstract reasoning and problem solving) is consistent with such an hypothesis, we believe an alternative hypothesis more fully explains the reduplication phenomenon. TABLE l.
Types of Primary Amnesias
Korsakoffs syndrome A . Korsakoff-type: (1) Disorientation (2) Confabulation (3) Integration amnesia
B. Registration-type: (4) Registration amnesia
x xa x
Reduplicative paramnesia
Hippocampal lesions
x xb x (x)
x
-------------------------------:----------a = unaware of contradictions b = aware of contradictions
On clinical evaluation, our patient's most evident problem is his inability to integrate recent observations with premorbid experience. We suggest that a disconnection of premorbid (past) memory stores from new memory registration is the essential functional impairment underlying reduplicative paramnesia (and perhaps Korsakoff's syndrome as well) . Such disconnection. a defect of memory association, would involve disconnection of the hippocampus from (certain) sites of past memory stores. Frontal lobe indifference, if present , might facilitate a continuing misinterpretation of reality. The most prominent clinical feature of reduplicative paramnesia is inaccurate orientation. Accurate orientation is a complex process requiring integration of a multiplicity of present cues with past experiences (Benson et aI., 1976; Gooddy, 1969). Our patient's duplications, like those of the three patients described by Benson et al. (1976), are duplications into the past (to a previous time, or to a previously occupied location) or are based upon the previous appearance of a person or object. The patients fail to integrate present cues in a manner permitting accurate orientation to present time and place . The basis of their current orientation is essentially a recollection from the past. Such orientation from past memory suggests that brain sites responsible for orientation are closer (anatomically or functionally) to stores of past experiences than to stores of recent memory (see figure 2). Kopelman (1979) has recently emphasized observations that recent and past memory are
R. Dennis Staton, Roger A. Brumback and Helen Wilson
32
necessary for accurate orientation time place
person
necessary for accurate orientation Fig. 2 - Postulated memory disconnection in reduplicative paramnesia producing orientation based upon past memories.
stored separately (Shallice and Warrington, 1970; Warrington and Rabin, 1971; Warrington, Logue and Pratt , 1971). Storage of past memory at sites distant from the hippocampi would make possible the anatomical disconnection postulated here. This formulation differs from the theory of O'Keefe and Nadel (1978) that the cognitive "map" providing spatial and temporal contexts for current cues resides in the right hippocampus. The deep right temporo-parieto-occipital junction is one location where a memory system disconnection producing disorientation could occur. Our CA T scan results, coupled with the neuropsychological impairment of visuospatial memory found in our patient and in that of Alexander et al. (1979), suggests this localization. Penfield and Mathieson (1974) report that the right temporal lobe is "frequently used. .. in interpretations of orientation in space". Many authors have reported severe memory disorders associated with occipital lesions (reviewed by Angelergues, 1969). These occipital lesions (in contrast to purely hippocampal and frontal lesions) are often associated with various forms of memory impairment plus disorientation and confabulation. Angelergues stresses that "disintegration of visual data could suffice to upset the time-space coordinates ot the individual" (1969, page 286. italics added) . Disruption of occipito-hippocampal association connections might disconnect past from present visual memories. producing disorientation and a primary amnesia of Korsakoff-type , such as reduplicative paramnesia. Perhaps the greater the extent of temporo-parieto-occipital injury. the more likely that reduplicative paramnesia will involve inaccurate orientation in multiple spheres, including time. The right temporo-parieto-occipitaI junction may be the primary association cortex responsible for orientation. Recent authors have attributed Capgras duplications to the presence of
Reduplicative paramnesia
33
prosopagnosia (Hayman and Abrams, 1977; Granacher, 1978; Shraberg and Weitzel, 1979). Although we attach some importance to impairments of visuospatial perception (such as prosopagnosia) in relation to orienting brain function, we stress the significance of memory disruption for the genesis of duplications. Attributing duplications to prosopagnosia provides an inadequate explanation for reduplicative paramnesia, even if prosopagnosia is occasionally present. Reversible disconnections should be possible and may explain the transient duplications associated with cerebral edema, metabolic encephalopathy, seizure activity, and "functional" psychosis (Alexander et al., 1979; Weinstein, 1969; Weston and Whitlock, 1971; McCallum, 1973; Benson et aI., 1976; Merrin and Silberfarb, 1976; Hayman and Abrams, 1977; Christodoulou, 1978; Nikolovski and Fernandez, 1978). Persisting reduplicative paramnesia probably requires brain atrophy and irreversible disconnection. Duplications are commonly considered symptoms of schizophrenic psychosis and treated with antipsychotic medication. We observed that our patient's sense of "unreality", which we attribute to disorientation and not to schizophrenia, was worsened by high dose L-dopa challenge and improved by dopamine-receptor blockade (antipsychotic chemotherapy). If impaired memory and orientation produce duplication phenomena, then these drug effects suggest that memory association must be functionally related to the dopaminergic meso limbic system (an observation compatible with recent studies of septal memory function by Winson, 1978, and Berry and Thompson, 1979). Such drug effects also suggest that so-called "functional" psychosis may at times be closely related to disorientation. The personality of our patient apparently changed asia consequence of right temporal brain damage and the resultant sense of unreality about himself and the world. His new personality traits of: (1) suspiciousness and a guarded approach to social relationships, (2) feeling victimized and angry, and (3) diminished frustration tolerance and impulse control (with increased aggressivity) are similar to those seen in immature, aggressive personality disorders (DSM-III, 301. 70 and 301.83). Brain injury which impairs orientation (reality testing) may be an important cause of immature behaviors.
ABSTRACT
A case of post-traumatic reduplicative paramnesia (Capgras syndrome) is presented in which the patient experiences duplications in all three spheres of orientation (time, place, person). We postulate that these duplications are the result of a disconnection of new memory registration from past memory stores. The patient is unable to integrate present cues with pre morbid experience, and bases judgements of his present orientation upon recollections from the past. A deep lesion at the right posterior hippocampus and temporo-parieto-occipital junction is suggested as the site of this postulated primary memory disconnection, based upon neuropsychologi-
34
R. Dennis Staton, Roger A . Brumback and Helen Wilson
cal testing and CAT scan results . This right temporal atrophy and memory disconnection appears to have induced immature personality changes.
Acknowledgement. This work was supported by the Veterans Administration . Roger Gilbertson. M.D .. and Lee Christoferson. M.D .. assisted with the patient evaluation . Garv Baune and David Rooerts assisted with the figure preparation. REFERENCES ABRAMS. R. (1977) Capgras syndrome (letter to the editor). Brit. J. Psychiat .. /31. 550-55\. ALEXANDER . M . P .. STUSS. D . T.. and BENSON . D . F . (1979) Capgras syndrome: a reduplicative phenomenon. Neurology. 29. 334-339. ANGElERGUES. R. (1969) Memory disorders in neurological disease. Chapter 16. pp. 268-292. in Handbook of Clinical Neurology. Volume 3. Disorders of Higher Nervous Activity. ed . by P. J. Vinken and G. W . Bruyn. North-Holland. Amsterdam . BEAR. D. M .. and FEOIO. P . (1977) Quantitative analysis of interictal behavior in temporal lobe epilepsy. Arch. Neurol. . 34.454-467. BENSON . D. F . . GARDNER. H .. and MEADOWS . 1. C. (1976) Reduplicative paramnesia . Neurology. 26.147-151. BERRY. S. D .. and THOMPSON. R. F. (1979) Medial septallesions retard classical conditioning of the nictitating membrane response in rablJits. Science. 205.209-211. CAPGRAS. J .. and REBOUL-L'ACHAU X. J. (1923) Illusion des sosies dans un delire systematist! chronique. Bull . Societe Clinique de Medicine Mentale.l . 0-10. CHRISTODOULOU . G. N. (1978) Course and prognosis of the syndrome of doubles. J. Nerv. Ment. Dis .. 166.68-72. Diagnostic and Statistical Manual of Mental Disorders. Third Edition (1980) Washington. D. c.: The American Psychiatric Association . GOODDY. W. (1969) Orientation. General introduction. physiological and psychological aspects. Chapter 11. pp . 202-211. in Handbook of Clinical Neurology. Vol. 3. Disorders of Higher Nervous Activity. ed. by P.J. Vinken and G.W . Bruyn. North-Holland . Amsterdam. GRANACHER. R.P. (1978) The Capgrassyndrome in old age. Amer. J. Psychiat . . 135.758-759. GR ONTHAL. E . (1947) Uber das klinische Bild nach umschriebenem beiderseitig im Ausfall der Ammonsshornrinde. Ein Beitrag zur Kenntnis der Funktion des Ammonshorns. Mschr. Psychiat. Neurol.. 113. 1-16. HAYMAN. M. A .. and ABRAMS. R. (1977) Capgras' syndrome and cerebral dysfunction. Brit. 1. Psychiat.. 130. 68-71. KOPElMAN. M. (1979) Memory (letter to the editor). Lancet. 1.666-667. LEZAK. M. D. (1976) Neuropsychological Assessment. Oxford University Press. New York. MACCALLUM. W .A .G . (1973) Capgras'symptoms with an organic basis. Brit. 1. Psychiat..123 . 1'i39-M2 . MI ~~IN. c.L.. and S" RFRFARB. P.M. (IY70) The Capgras phenomenon. Arch. Gen. Psychiat.. 33. Y65-Y68, MILNER. B. (1958) Psychological defects produced by temporal lobe excisions . Res. Pub!. Ass. Res. Nerv. Ment. Dis .. 36. 224-240. - (1962) Laterality effects in audition. Interhemispheric Rela tions and Cerebral Dominance . ed . by V. B. Mountcastle . Johns Hopkins University Press. Baltimore. ( 19(5) Visually guided maze learning in man: effects of bilateral hippocampal, bilateral frontal and unilateral cerebral lesions. Neuropsychologia (Oxford). 3. 317-338. ( 1968) Visual recognition and recall after right temporal lobe excision in man. Neuropsychologia (Oxford). 6.191-209. NI"()I()\'oKI. O. T.. and FF~NAND EZ . J. V . (IY7S) Capgras syndrome as an aftermath of chickenpox encephalitis. Psychiatric Opinion. Feb .. 39-43 . O·KEEFE. J .. and NADEL. L. (1978) The Hippocampus as a Cognitive Map. Oxford University Press . New York .
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PENFIELD. W.E .. and MATHIFSON. G. (IY7.+) Memorv: autopsv findings and comments on the role of hippocampus in experiential recall. Arch. Neurol.. 31. 145-154. - . and MILNER. B. (1958) Memory deficit produced by bilateral lesions in the hippocampal zone. Arch. Neurol. Psychiat.. 79.475-497. PICK. A. (1903) Clinical Studies: III. On reduplicative paramnesia. Brain. 26. 260-267. REITAN. R. M. (1964) Psychological deficits resulting from cerebral lesions in man. in The Frontal Granular Cortex and Behavior. ed. by 1. M. Warren and K. Akert. McGraw-Hili. New York. RUSSELL. E. W .• NEURINGER. c.. and GOLDSTEIN. G. (1970) Assessment of Brain Damage: A Neuropsychological Key Approach. Wiley-Interscience. New York. SCOVILLE. W. B .. and MILNER. B. (1957) Loss of recent memory after bilateral hippocampal lesions. 1. Neurol. Neurosurg. Psychiat.. 20. 11-2l. SHALLICE .. and WARRINGTON. E. K. (1970) Independentfunctioningofverbal memory stores: a neuropsychological study. Quart. 1. Exp. Psycho\" 22. 261-273. SHRABERG. D .• and WEITZEL. W. D. (1979) Prosopagnosia and the Capgras syndrome. 1. CIin. Psychiatry. 40. 313-316. TEUBER. H.L.. and WEINSTEIN. S. (1954) Performance on a Formboard task after penetrating brain injury. 1. Psycho\" 38.177-190. WARRINGTON. E. K .. LoGUE. V .. and PRATI. R. T. (1971) The anatomical localization of selective impairment of auditory verbal short-term memory. Neuropsychologia. 9. 377-387. - . and RABIN. P. (\ (71) Visual span of apprehension in patients with unilateral cerebral lesions. Quart. 1. Exp. Psychol.. 23. 423-431. WEINSTEIN. E. A. (1969) Patterns of reduplication in organic brain disease. Chapter 14. pp. 251-257. in Handbook of Clinical Neurology. Vol. 3. Disorders of Higher Nervous Activity. ed. by P. 1. Vinken and G. W. Bruyn. North-Holland, Amsterdam. WESTON. M. 1. and WHITLOCK. F. A. (1971) The Capgras syndrome following head injury. Brit. 1. Psychiat.. 119. 25-3l. WINSON. 1. (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science. 201. HiO-163. R.A. Brumback -The University of North Dakota -School of Medicine 1919 Elm Street North. FARGO. NO. 58102 USA.
INTRODUCTION
The Capgras syndrome (Capgras and Reboul-L'achaux, 1923) is characterized by failure to recognize a familiar person (or persons), associated with belief that the real person has been replaced by a double. This syndrome is a variant of the phenomenon of reduplicative paramnesia (Pick, 1903), which may include duplication (called reduplication by Pick) not only of familiar people but also of self, of places, and of time and events (Abrams, 1977; Alexander, Stuss and Benson, 1979; Weinstein, 1969). Even though Capgras symptoms have typically been attributed to functional psychosis. a variety of organic brain lesions have been shown to produce duplication syndromes (Alexander et al., 1979; Weinstein, 1969; Weston and Whitlock. 1971; MacCallum, 1973; Benson, Gardner and Meadows, 1976; Merrin and Silberfarb. 1976; Hayman and Abrams. 1()77; Christodoulou. 1()7H; Nikolovski and Fernandez, 1978). Although Pick used the term paramnesia to indicate that the duplication symptoms were related to a disturbance of memory, recent authors have focused upon visual perceptual problems, including prosopagnosia (Alexander et al., 1979; Benson et al.. 1976; Hayman and Abrams, 1977; Granacher. 1978; Shraberg and WeitzeL 1979). and/or frontal lobe apathy (Alexander et al., 1979; Benson et al., 1976) as an explanation of duplication syndromes. We agree with Pick, that the central pathology of these syndromes is a disturbance of memory. We describe a case of post-traumatic reduplicative paramnesia in which the symptoms appear to derive from impairment of integration of newly acquired information with older memories. lPresented in part at the Second European Conference of the International Neuropsychology Society, Noordwijkerhout. Holland. June 30. 1979. Cortex (1982) 18, 23-36.
24
R. Dennis Staton, Roger A. Brumback and Helen Wilson
CASE REpORT
The patient, RK, with no prior history of psychiatric or neurologic impairment. was found unconscious on July 25, 1970, at age 23 years, after a single-car accident. On admission to the hospital, x-ray studies revealed no skull fracture. He remained comatose for seven days, but then made a rapid recovery and was discharged on the 25th hospital day. Repeat neurologic examinations during the years following his accident have shown very slight left hyper-reflexia, left extensor plantar response (Babinski reflex), and a mild left central facial nerve palsy. Gait unsteadiness present for several months after the accident has resolved. Visual fields are normal. Three electroencephalograms done since the accident have demonstrated right te~poral slowing. Four-vessel cerebral angiography performed eight years after the aCCident showed no abnormality. The results of computerized axial tomographic (C AT) scanning also done eight years post-accident are described below. Two months after the accident the patient was referred for neurosurgical evaluation of left hand "numbness" (now resolved) and a change in personality. At that time, his parents reported that approximately five weeks after the accident RK developed new and uncharacteristic behaviors. He became persistently irritable and angry, with temper outbursts and an uncooperative and belligerent attitude. Examination at that time revealed retrograde amnesia and difficulty learning new information . With the exception of these reported impairments of personality and memory, and a very slight gait impairment, RK was considered by his neurosurgeon to have made an excellent recovery from his head injury. Two years after the accident the patient unsuccessfully attended business college, attributing his failure to difficulty with memory. In the first months after his accident, RK experienced feelings of "unreality" . These feelings persisted, but were not reported by RK to his physician until 1974, four years after his accident, when he was hospitalized because of his explosive temper. His parents reported then that RK had developed additional problems of feeling victimized, blaming others, and social withdrawal. These factors, along with his persisting poor frustration tolerance and impulse control, had contributed to numerous employment failures and repeated conflicts with his family. During the 1974 hospitalization, RK described a conviction that all of his current experiences had happened before . His condition was described as deja vu by psychiatric and psychologic consultants, who considered his emotional problems " psychogenic" in origin. On referral to us in October 1978, eight years after his accident, RK was age 31, unmarried and unemployed. He felt desperate and described living in a world that ' seemed to be a fantasy. He stated that "everything is so different" (than before the accident). Friends .and relatives, including his parents and siblings, were not "real" - but were slightly different " look-alikes", or doubles - not the real people he had known before the accident . This was also true of places, including the family farm and the city where he was hospitalized. "They didn't have this kind of hospital in Fargo . I must be somewhere else." He did not know where he was. He didn't know where his true relatives were, but he was sure that the present "relatives" were false duplicates. He recognized them as duplicates through differences between their current behavior (or appearance) and his recollections from the past. "This person cannot be my cousin because my real cousin worked at a different job." The family farm was a false duplicate because recently added buildings "don't seem as if they should have been built." His cat was not real because of a new scar on one ear. He even denied that he could be the true RK because several aspects of his present appearance (including a lost tooth and a foot callus) were different than he remem-
Reduplicative paramnesia
25
bered. "If I were really me I'd have a place of my own. I'd be working." In spite of being able to recount evidence to the contrary, he believed that he had not actually lived in a certain city for two years after the accident. "I would never do that!" He referred to his parents as "those people". His father could not be real because "he has tractors that my (real) father wouldn't have bought." "He wouldn't have expanded the milk business." The unreal people, places, objects, and experiences were not perceived as exact duplicates. They were all slightly different from past appearance or recollection. These differences between his present observations and his past memory provided the evidence for duplication. He stated that "the problem is that my memory is too good. " He had no difficulty identifying objects. RK described several elaborate delusions (or confabulations) which eased the desperation of his "unreal" life. He believed that the entire eight-year period of disability and "unreality" lived since the accident had really occurred some time previously and had culminated in complete recovery. He expected his current reliving of past life experiences, although entirely unreal, to have the same optimistic outcome (that is, he would recover). It was in this context that all current experiences seemed to be false duplications of similar previous experiences. RK also believed that the present time could not be October 1978. It was "approximately 1975", because: (1) his physician had told him that he would be "nearly back to normal", married, and working by the time he was age 30 (which would be the year 1977); and (2) his old girlfriend, who had recently married someone else, would still be single if it were 1975. Consistent with this disorientation to time, he denied the reality of recent world events. RK stated that "I can't trust anything." "I don't have control over things that are happening to me." Although RK was very suspicious, he had no paranoid conviction of a plot against him. A moderately severe reactive depression was present. manifested by depressed affect, low self-esteem, pessimism regarding the future, and a feeling that he might be better off dead. There was no evidence suggesting the presence of a delusional endogenous depression, schizophrenia, drug toxicity, or exceptional situational stress. We considered RK to be psychotic, in that he maintained irrational beliefs, and we attributed this psychosis to his structural brain injury. RK had been medicated at different times during the preceding four years with the dopamine-blocking agents trifluoperazine 2 mg t.i.d. and haloperidol 1 mg t.i.d .. without benefit. In spite of these failures. we decided to assess the possibility of a dopaminergic basis to RK's psychosis with a 23-day trial of combination carbidopa/L-dopa 25 mg /250 mg tablets, with doses increasing to a maximum of 8 tablets per day. On this regimen he showed progressively worsening symptomatology, and after three days on the maximal dosage he reported that: "Things are even more unreal. I feel totally out of place. There isn't any such place as this. I don't believe this. I don't believe this is a real hospital." The carbidopa/L-dopa was stopped and RK was subsequently given fluphenazine hydrochloride. He showed marked symptomatic improvement four days after the dosage of fluphenazine hydrochloride had reached 12.5 mg per day. Both his duplication experiences and his SUbjective distress were lessened. His family members were now perceived as real. He explained his previous inability to recognize family members by stating: "I remember them differently." He remained slightly troubled by some behaviors of family members, feeling that they were doing things that they "shouldn't be doing" (according to his past memory of them). His disorientation for time also persisted.
26
R . Dennis Staton, Roger A. Brumback and Helen Wilson
CAT SCAN RESULTS
CAT scanning performed November L 1978, revealed the following lesions (Figure 1): (1) atrophy in the region of the posterior right hippocampus and adjacent temporal lobe. (2) a discrete area of moderate atrophy deep in the posterior-superior temporal lobe at the temporo-parietal junction, in a region traversed by occipito-temporal fibers, (3) mild atrophy at the right parieto-occipital junction, (4) mild peri-Sylvian atrophy of the right posterior frontal operCUlum, and (5) mild, diffuse frontal lobe atrophy. NEUROPSYCHOLOGICAL Ev ALUATION
Behavioral Observations RK appeared at the appointed time for the current test battery, but expressed ambivalence about the procedure. He was suspicious, questioning each test and the consequences of responding. His experiences following the accident were related with a bland lack of concern during the evaluation interview. Despite apparent hostility, he completed all tasks and seemed motivated to perform well. At the time of this neuropsychological evaluation , RK was receiving no medication.
Fig. I - CA T scan sections showing atrophy in the region of the posterior right hippocampus and adjacent temporal lobe, and atrophy in the right posterior-superior temporal lobe at the temporo-parietal junction.
Reduplicative paramnesia
27
Intelligence Testing Wechsler Adult Intelligence Scale (WAIS) testing conducted 2 months after RK's accident and repeated 8 years later showed Verbal IQs of 93/106, Performance IQs .of 72/95, and Full Scale IQs of 83/102. Improvement occurred in overall intellectual capability, particularly in nonverbal skills, although a mild Verbal-Performance discrepancy remained. This persistent Performance IQ deficit suggests a right hemisphere disturbance involving primarily nonverbal cognitive functions, with the relatively lower scores on Digit Symbol, Block Design, and Object Assembly sub tests (on current testing) suggesting the presence of visual perceptive impairment.
Memory Testing Memory was tested using the Wechsler Memory Scale (WMS), the Graham-Kendall Memory-For-Designs, and the Benton Visual Retention Test. RK's Memory Quotient was 90. His poor performance on the Logical Memory sub test of the WMS suggested mild concentration, integration, and/or retrieval deficit. The most significant deficiencies were found in short term visual memory and reproduction of designs.
Neuropsychological Battery RK showed mild to moderate impairments in nonverbal abstraction and problem-solving (Category Test), nonverbal auditory perception (Rhythm Test), tactual memory and motor problem solving (when using his left hand) on the Tactual Performance Test (TPT). Right hand performance on the TPT was normal. There was no evidence for a language disturbance on the Halstead-Reitan Aphasia Screening Test. There was some indication of a mild constructional apraxia in a task which involved copying a Greek cross. Speech perception was normal. These results provide supporting evidence of dysfunction in the right hemisphere, with primarily temporal lobe localization. The patient also showed deficient performance on the following tests: Porteus Mazes (performance deficits in ordering, planning, and foresight), Trails A and B (deficient visual sequencing and. motor speed), and the Finger Agnosia and Fingertip Writing subtests (impaired tactile preception) ..These results did not suggest lateralized dysfunction.
28
R. Dennis Staton, Roger A. Bmmback and Helen Wilson
Motor Tests All tests of motor skills, including finger tapping and grip strength, were in the normal to above average range.
Summary of Neuropsychological Testing Neuropsychological deficiencies were found in the following tests: Dysfunction
Test Revealing Deficit
1. Visuospatial (visual perceptive) skills
W AIS Performance Scale subtests Copying Greek cross
2. Visual memory and reproduction
Visual Reproduction subtest of the WMS Benton Visual Retention Graham-Kendall Memory-ForDesigns Seashore Rhythm Perception Test
3. Nonverbal auditory perception 4. Problem solving
Halstead Category Test Tactual Performance Test (TPT) Porteus Mazes (Vineland Revision)
This overall pattern of neuropsychological deficit is consistent with right hemisphere dysfunction, primarily of the posterior association cortex (Milner, 1958; Russell, Neuringer and Goldstein, 1970; Lezak, 1976). RK demonstrated difficulties with nonverbal auditory discrimination, a perceptual disorder associated with posterior right temporal lobe dysfunction (Milner, 1962), but did not show amusia, which is related to more anterior temporal lobe lesions. The TPT (particularly the memory component) relies heavily on nonverbal learning, which is considered a right hemispheric function. Teuber and Weinstein (1954) have shown that posterior right temporo-parietallesions (near the temporo-occipital boundary) may result in impaired performance on the TPT. Precentral (motor strip) frontal lobe damage can also impair TPT performance (Reitan, 1964), but such damage was not suggested by our motor testing. The deficits found on the Category Test (a measure of nonverbal abstraction) may be localized to the right temporal and/or frontal lobes. Involvement of occipital lobe function is suggested by impaired visual memory and perception. Since no primary visual deficit was evident in this patient, his occipital impairment seems to result from interruption of visual input to the temporal lobe. Thus, the functional deficits observed in this
Reduplicative paramnesia
29
patient are primarily in the right temporal lobe. Minor right parietal and fro n t'al lobe involvement is also suggested.
Personality Testing RK's parents have reported in clinical interviews since the accident that their son has manifested the following new traits: feeling victimized and blaming others, emotional irritability, anger, social withdrawal, dependence, and apathy. A behavior questionnaire developed by Bear and Fedio (1977), used to assess disturbances presumably related to limbic system dysfunction, was administered to our patient. On this questionnaire, as on the Minnesota Multiphasic Personality Inventory (MMPI), RK denied most abnormalities. A separate Bear-Fedio rater form was completed by the parents, who perceived RK as suspicious, angry, easily frustrated, emotional, aggressive, depressed, and repetitive in his thinking. MMPI and projective drawing tests were administered to RK at the time of neuropsychological evaluation. Interpretation of RK's MMPI profile is complicated by marked elevations on the validity scales. The F-K index (-16), along with the high L Scale (= 70), strongly suggests excessive denial of emotional problems and an intense need to present a good image. The profile configuration showed elevations on Scales 4 and 8 indicating general social maladjustment. Personality traits compatible with the 4-~ configuration and found in RK include immaturity, low self-esteem, feeling victimized and blaming others, anger, suspiciousness, feelings of alienation, and social isolation. Testing also revealed authority conflicts and complaints against family. The most striking findings in RK's MMPI data and his projective tests are: (1) a high degree of suspiciousness, (2) a guarded approach to social relationships, (3) marked isolation and constricted expression of emotions, and (4) a sense of unreality about himself and the world. Repeat MMPI testing after six months of therapy with fluphenazine hydrochloride revealed a reduction in the intensity of these traits, with Scales 4 and 8 reduced to within the normal range. DISCUSSION
The patient described in this report has reduplicative paramnesia (Pick 1903), including Capgras symptoms (Capgras and Reboul-L'achaux, 1923). Weinstein has reviewed the phenomenon of reduplication, which may include duplication of time and events, of place, of person, of self, of body parts (usually the non-dominant upper extremity), and of objects (Weinstein, 1969). Such duplications result from brain injury of various causes (Alexanderet al., 1979; Weinstein, 1969; Weston and Whitlock, 1971;
30
R. Dennis Staton, Roger A. Brumback and Helen Wilson
MacCallum, IY73;Bensonetal., IY76;MerrinandSilberfarb, 1976; Hayman and Abrams, 1977; Christodoulou, 1978; Nikolovski and Fernandez, 1978). Our patient suffered closed head trauma and subsequently manifested duplications of place, of person (including self), of time and events, and of certain objects. Patients with reduplicative paramnesia frequently explain their duplication(s) with confabulation: an irrational explanation occurring in the presence of memory dysfunction (Weinstein, 1969). Our patient's delusional explanation that his current predicament derives from his living in a "fantasy world" (described in the case report) represents such a confabulation. Reduplicative paramnesia may bear a relationship to primary amnesia. Angelergues (1969) defines two basic aspects of primary amnesia. One aspect is Korsakoff's syndrome, resulting from lesions of diencephalic areas or the memory circuit 2 , or, less commonly, from lesions of the occipital cortex. Angelergues considers Korsakoff's syndrome to include three elements, all of which are demonstrable in our patient: (1) disorientation, (2) confabulation, and (3) amnesia in the special sense of inability to integrate present and past memories. Our patient's disorientation is manifested by failure to recognize family members, certain places, and present time as real. His explanation of the duplications is confabulatory, as previously described. Like the patients reported by Alexander et ai. (1979) and Benson et ai. (1 Y76), our patient is able to register new information, but fails to integrate. this new memory with past memory. While we do not equate reduplicative paramnesia with Korsakoff's syndrome, the reduplication phenomenon does appear to satisfy criteria for inclusion as a primary amnesia analogous to Korsakoff's syndrome. Thus, patients with both reduplicative paramnesia and Korsakoff's syndrome are disoriented, frequently confabulate, and experience difficulty comparing and integrating present cues with past experience (see Table I). The striking difference between these disorders is that with reduplicative paramnesia the patient is aware of contradictions (related to the duplication), while such awareness is absent in Korsakoff's syndrome (Grunthal, 1947). The second basic aspect of primary amnesia defined by Angelergues (1969) is amnesia of registration of new information, resulting primarily from hippocampal lesions (Scoville and Milner, 1957; Penfield and Milner, 1958; Milner, 1965; Milner, 1968; Penfield and Mathieson, 1974). Our patient shows impaired registration of visuospatial memory (perhaps explained by the posterior hippocampal atrophy demonstrable by CAT scan). Similar visuospatial impairment, along with frontal lobe impairment, was noted in the patient reported by Alexander et al. (1979), and these authors attributed 2The memory circuit described by Angelergues (1969) includes Ammons horn, fornix. hypothalamus. mammillary bodies, bundle of Vicq d'Azyr, anterior thalamic nuclei, and cingulum.
Reduplicative paramnesia
31
their patient's persisting duplication of place to the frontal lobe damage . Although our finding of minor frontal lobe atrophy by CAT scan (and midly impaired abstract reasoning and problem solving) is consistent with such an hypothesis, we believe an alternative hypothesis more fully explains the reduplication phenomenon. TABLE l.
Types of Primary Amnesias
Korsakoffs syndrome A . Korsakoff-type: (1) Disorientation (2) Confabulation (3) Integration amnesia
B. Registration-type: (4) Registration amnesia
x xa x
Reduplicative paramnesia
Hippocampal lesions
x xb x (x)
x
-------------------------------:----------a = unaware of contradictions b = aware of contradictions
On clinical evaluation, our patient's most evident problem is his inability to integrate recent observations with premorbid experience. We suggest that a disconnection of premorbid (past) memory stores from new memory registration is the essential functional impairment underlying reduplicative paramnesia (and perhaps Korsakoff's syndrome as well) . Such disconnection. a defect of memory association, would involve disconnection of the hippocampus from (certain) sites of past memory stores. Frontal lobe indifference, if present , might facilitate a continuing misinterpretation of reality. The most prominent clinical feature of reduplicative paramnesia is inaccurate orientation. Accurate orientation is a complex process requiring integration of a multiplicity of present cues with past experiences (Benson et aI., 1976; Gooddy, 1969). Our patient's duplications, like those of the three patients described by Benson et al. (1976), are duplications into the past (to a previous time, or to a previously occupied location) or are based upon the previous appearance of a person or object. The patients fail to integrate present cues in a manner permitting accurate orientation to present time and place . The basis of their current orientation is essentially a recollection from the past. Such orientation from past memory suggests that brain sites responsible for orientation are closer (anatomically or functionally) to stores of past experiences than to stores of recent memory (see figure 2). Kopelman (1979) has recently emphasized observations that recent and past memory are
R. Dennis Staton, Roger A. Brumback and Helen Wilson
32
necessary for accurate orientation time place
person
necessary for accurate orientation Fig. 2 - Postulated memory disconnection in reduplicative paramnesia producing orientation based upon past memories.
stored separately (Shallice and Warrington, 1970; Warrington and Rabin, 1971; Warrington, Logue and Pratt , 1971). Storage of past memory at sites distant from the hippocampi would make possible the anatomical disconnection postulated here. This formulation differs from the theory of O'Keefe and Nadel (1978) that the cognitive "map" providing spatial and temporal contexts for current cues resides in the right hippocampus. The deep right temporo-parieto-occipital junction is one location where a memory system disconnection producing disorientation could occur. Our CA T scan results, coupled with the neuropsychological impairment of visuospatial memory found in our patient and in that of Alexander et al. (1979), suggests this localization. Penfield and Mathieson (1974) report that the right temporal lobe is "frequently used. .. in interpretations of orientation in space". Many authors have reported severe memory disorders associated with occipital lesions (reviewed by Angelergues, 1969). These occipital lesions (in contrast to purely hippocampal and frontal lesions) are often associated with various forms of memory impairment plus disorientation and confabulation. Angelergues stresses that "disintegration of visual data could suffice to upset the time-space coordinates ot the individual" (1969, page 286. italics added) . Disruption of occipito-hippocampal association connections might disconnect past from present visual memories. producing disorientation and a primary amnesia of Korsakoff-type , such as reduplicative paramnesia. Perhaps the greater the extent of temporo-parieto-occipital injury. the more likely that reduplicative paramnesia will involve inaccurate orientation in multiple spheres, including time. The right temporo-parieto-occipitaI junction may be the primary association cortex responsible for orientation. Recent authors have attributed Capgras duplications to the presence of
Reduplicative paramnesia
33
prosopagnosia (Hayman and Abrams, 1977; Granacher, 1978; Shraberg and Weitzel, 1979). Although we attach some importance to impairments of visuospatial perception (such as prosopagnosia) in relation to orienting brain function, we stress the significance of memory disruption for the genesis of duplications. Attributing duplications to prosopagnosia provides an inadequate explanation for reduplicative paramnesia, even if prosopagnosia is occasionally present. Reversible disconnections should be possible and may explain the transient duplications associated with cerebral edema, metabolic encephalopathy, seizure activity, and "functional" psychosis (Alexander et al., 1979; Weinstein, 1969; Weston and Whitlock, 1971; McCallum, 1973; Benson et aI., 1976; Merrin and Silberfarb, 1976; Hayman and Abrams, 1977; Christodoulou, 1978; Nikolovski and Fernandez, 1978). Persisting reduplicative paramnesia probably requires brain atrophy and irreversible disconnection. Duplications are commonly considered symptoms of schizophrenic psychosis and treated with antipsychotic medication. We observed that our patient's sense of "unreality", which we attribute to disorientation and not to schizophrenia, was worsened by high dose L-dopa challenge and improved by dopamine-receptor blockade (antipsychotic chemotherapy). If impaired memory and orientation produce duplication phenomena, then these drug effects suggest that memory association must be functionally related to the dopaminergic meso limbic system (an observation compatible with recent studies of septal memory function by Winson, 1978, and Berry and Thompson, 1979). Such drug effects also suggest that so-called "functional" psychosis may at times be closely related to disorientation. The personality of our patient apparently changed asia consequence of right temporal brain damage and the resultant sense of unreality about himself and the world. His new personality traits of: (1) suspiciousness and a guarded approach to social relationships, (2) feeling victimized and angry, and (3) diminished frustration tolerance and impulse control (with increased aggressivity) are similar to those seen in immature, aggressive personality disorders (DSM-III, 301. 70 and 301.83). Brain injury which impairs orientation (reality testing) may be an important cause of immature behaviors.
ABSTRACT
A case of post-traumatic reduplicative paramnesia (Capgras syndrome) is presented in which the patient experiences duplications in all three spheres of orientation (time, place, person). We postulate that these duplications are the result of a disconnection of new memory registration from past memory stores. The patient is unable to integrate present cues with pre morbid experience, and bases judgements of his present orientation upon recollections from the past. A deep lesion at the right posterior hippocampus and temporo-parieto-occipital junction is suggested as the site of this postulated primary memory disconnection, based upon neuropsychologi-
34
R. Dennis Staton, Roger A . Brumback and Helen Wilson
cal testing and CAT scan results . This right temporal atrophy and memory disconnection appears to have induced immature personality changes.
Acknowledgement. This work was supported by the Veterans Administration . Roger Gilbertson. M.D .. and Lee Christoferson. M.D .. assisted with the patient evaluation . Garv Baune and David Rooerts assisted with the figure preparation. REFERENCES ABRAMS. R. (1977) Capgras syndrome (letter to the editor). Brit. J. Psychiat .. /31. 550-55\. ALEXANDER . M . P .. STUSS. D . T.. and BENSON . D . F . (1979) Capgras syndrome: a reduplicative phenomenon. Neurology. 29. 334-339. ANGElERGUES. R. (1969) Memory disorders in neurological disease. Chapter 16. pp. 268-292. in Handbook of Clinical Neurology. Volume 3. Disorders of Higher Nervous Activity. ed . by P. J. Vinken and G. W . Bruyn. North-Holland. Amsterdam . BEAR. D. M .. and FEOIO. P . (1977) Quantitative analysis of interictal behavior in temporal lobe epilepsy. Arch. Neurol. . 34.454-467. BENSON . D. F . . GARDNER. H .. and MEADOWS . 1. C. (1976) Reduplicative paramnesia . Neurology. 26.147-151. BERRY. S. D .. and THOMPSON. R. F. (1979) Medial septallesions retard classical conditioning of the nictitating membrane response in rablJits. Science. 205.209-211. CAPGRAS. J .. and REBOUL-L'ACHAU X. J. (1923) Illusion des sosies dans un delire systematist! chronique. Bull . Societe Clinique de Medicine Mentale.l . 0-10. CHRISTODOULOU . G. N. (1978) Course and prognosis of the syndrome of doubles. J. Nerv. Ment. Dis .. 166.68-72. Diagnostic and Statistical Manual of Mental Disorders. Third Edition (1980) Washington. D. c.: The American Psychiatric Association . GOODDY. W. (1969) Orientation. General introduction. physiological and psychological aspects. Chapter 11. pp . 202-211. in Handbook of Clinical Neurology. Vol. 3. Disorders of Higher Nervous Activity. ed. by P.J. Vinken and G.W . Bruyn. North-Holland . Amsterdam. GRANACHER. R.P. (1978) The Capgrassyndrome in old age. Amer. J. Psychiat . . 135.758-759. GR ONTHAL. E . (1947) Uber das klinische Bild nach umschriebenem beiderseitig im Ausfall der Ammonsshornrinde. Ein Beitrag zur Kenntnis der Funktion des Ammonshorns. Mschr. Psychiat. Neurol.. 113. 1-16. HAYMAN. M. A .. and ABRAMS. R. (1977) Capgras' syndrome and cerebral dysfunction. Brit. 1. Psychiat.. 130. 68-71. KOPElMAN. M. (1979) Memory (letter to the editor). Lancet. 1.666-667. LEZAK. M. D. (1976) Neuropsychological Assessment. Oxford University Press. New York. MACCALLUM. W .A .G . (1973) Capgras'symptoms with an organic basis. Brit. 1. Psychiat..123 . 1'i39-M2 . MI ~~IN. c.L.. and S" RFRFARB. P.M. (IY70) The Capgras phenomenon. Arch. Gen. Psychiat.. 33. Y65-Y68, MILNER. B. (1958) Psychological defects produced by temporal lobe excisions . Res. Pub!. Ass. Res. Nerv. Ment. Dis .. 36. 224-240. - (1962) Laterality effects in audition. Interhemispheric Rela tions and Cerebral Dominance . ed . by V. B. Mountcastle . Johns Hopkins University Press. Baltimore. ( 19(5) Visually guided maze learning in man: effects of bilateral hippocampal, bilateral frontal and unilateral cerebral lesions. Neuropsychologia (Oxford). 3. 317-338. ( 1968) Visual recognition and recall after right temporal lobe excision in man. Neuropsychologia (Oxford). 6.191-209. NI"()I()\'oKI. O. T.. and FF~NAND EZ . J. V . (IY7S) Capgras syndrome as an aftermath of chickenpox encephalitis. Psychiatric Opinion. Feb .. 39-43 . O·KEEFE. J .. and NADEL. L. (1978) The Hippocampus as a Cognitive Map. Oxford University Press . New York .
Reduplicative paramnesia
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