Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-25T17:11:03.112Z Has data issue: false hasContentIssue false
  • English
  • Français

Learning and memory in monozygotic twins discordant for schizophrenia

Published online by Cambridge University Press:  09 July 2009

Terry E. Goldberg ,
E. Fuller Torrey ,
James M. Gold ,
J. Daniel Ragland ,
Llewellyn B. Bigelow  and
Daniel R. Weinberger
Terry E. Goldberg*
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
E. Fuller Torrey
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
James M. Gold
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
J. Daniel Ragland
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
Llewellyn B. Bigelow
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
Daniel R. Weinberger
Affiliation:
Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, Washington, DC, USA
*
1Address for correspondence: Dr Terry E. Goldberg, Clinical Brain Disorders Branch, Intramural Research Program, National Institute of Mental Health, Neuroscience Center at Saint Elizabeths, 2700 Martin Luther King Jr. Avenue, SE, Washington, DC 20032, USA.
Get access Rights & Permissions [Opens in a new window]

Synopsis

Learning and memory were assessed in 24 monozygotic (MZ) pairs of individuals discordant for schizophrenia or delusional disorder and seven normal pairs of MZ twins. On declarative memory tasks, the affected group displayed a pattern that might best be characterized as dysmnesic in that they performed significantly worse than the discordant unaffected group on story recall, paired associated learning, and visual recall of designs, but they learned over time, had relatively preserved recognition memory, and did not show profoundly accelerated rates of forgetting. Effortful, volitional retrieval from the lexicon, measured by verbal fluency, was also compromised in the affected group. On the other hand, procedural learning of the motor skill in a pursuit rotor task was relatively intact in the affected group. Comparisons of the normal group and unaffected group indicated that the latter group had very mild impairments in some aspects of episodic memory, namely, immediate and delayed recall of stories and delayed recall of designs. It is highly unlikely that the impairments observed in the affected group can be attributed to differences in genome, family environment, socioeconomic circumstance, or educational opportunity, as all of these were controlled by the twin paradigm. Rather, the impairments appear to be related to the intercession of disease. The neuropsychological profile is consistent with frontal lobe and medial temporal lobe dysfunction, as noted in this sample as well as other samples of schizophrenic singletons. Significant correlations between many measures of memory and global level of social and vocational functioning within the discordant group were also found. Thus difficulties in rapidly acquiring new information and propitiously retrieving old information may burden patients with schizophrenia in many of the transactions of everyday life.

Type
Original Articles
Information
Psychological Medicine , Volume 23 , Issue 1 , February 1993 , pp. 71 - 85
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Andreasen, N. C. (1981). Scales for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City, IA.Google Scholar
Baddeley, A. (1986). Working Memory. Oxford University Press: New York.Google ScholarPubMed
Baddeley, A. D. & Warrington, E. D. (1970). Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior 9, 176–189.CrossRefGoogle Scholar
Bauman, E. & Murray, D. J. (1968). Recognition versus recall in schizophrenia. Canadian Journal of Psychology 22, 18–25.CrossRefGoogle ScholarPubMed
Benton, A. L. (1968). Differential behavioral effects in frontal lobe disease. Neuropsychologia 6, 53–60.CrossRefGoogle Scholar
Berman, K. F., Torrey, E. F. & Weinberger, D. R. (1992). rCBF in monozygotic twins discordant for schizophrenia. Archives of General Psychiatry (in the press).CrossRefGoogle Scholar
Bogerts, B., Meertz, E. & Schonfeld-Bausch, R. (1985). Basal ganglia and limbic system pathology in schizophrenia: A morphometric study. Archives of General Psychiatry 42, 784–791.CrossRefGoogle ScholarPubMed
Brown, R., Colter, N., Corsellis, J. A. N., Crow, T. J., Frith, C. D., Jagoe, R., Johnstone, E. C. & Marsh, L. (1986). Postmortem evidence of structural brain changes in schizophrenia. Archives of General Psychiatry 43, 36–42.CrossRefGoogle ScholarPubMed
Butters, N., Wolfe, J., Martone, M., Granholm, E. & Cermak, L. S. (1985). Memory disorders associated with Huntington's disease: verbal recall, verbal recognition and procedural memory. Neuropsychologia 23, 729–743.CrossRefGoogle ScholarPubMed
Calev, A. (1984). Recall and recognition in mildly disturbed schizophrenics: the use of matched tasks. Psychological Medicine 14, 425–429.CrossRefGoogle ScholarPubMed
Calev, A. & Monk, A. F. (1982). Verbal memory tasks showing no deficit in schizophrenia – fact or artefact? British Journal of Psychiatry 141, 528–530.CrossRefGoogle ScholarPubMed
Calev, A., Berlin, H. & Lever, B. (1987). Remote and recent memory in long hospitalized schizophrenics. Biological Psychiatry 22, 79–85.CrossRefGoogle Scholar
Chapman, L. J. & Chapman, J. P. (1973). Problems in the measurement of cognitive deficit. Psychological Bulletin 79, 380–385.CrossRefGoogle ScholarPubMed
Cutting, J. (1979). Memory in functional psychosis. Journal of Neurology, Neurosurgery, and Psychiatry 42, 1031–1037.CrossRefGoogle ScholarPubMed
Drachman, D. A. & Leavitt, J. (1974). Human memory and the cholinergic system. Archives of Neurology 30, 113–121.CrossRefGoogle ScholarPubMed
Frame, C. & Oltmanns, T. F. (1982). Serial recall by schizophrenic and affective patients during and after psychotic episodes. Journal of Abnormal Psychology 91, 311–318.CrossRefGoogle ScholarPubMed
Frisk, V. & Milner, B. (1990). The relationship of working memory to the immediate recall of stories following unilateral temporal frontal lobectomy. Neuropsychologia 28, 121–135.CrossRefGoogle Scholar
Frith, C. (1984). Schizophrenia, memory, and anticholinergic drugs. Journal of Abnormal Psychology 93, 339–341.CrossRefGoogle ScholarPubMed
Gold, J. M. & Hurt, S. W. (1990). The effects of haloperidol on thought disorder and IQ in schizophrenia. Journal of Personality Assessment 54, 390–400.CrossRefGoogle ScholarPubMed
Goldberg, T. E., Weinberger, D. R., Berman, K. F., Pliskin, N. H. & Podd, M. H. (1987). Further evidence for dementia of the prefrontal type of schizophrenia? Archives of General Psychiatry 44, 1008–1016.CrossRefGoogle ScholarPubMed
Goldberg, T. E., Berman, K. F. & Weinberger, D. R. (1989). An orientation to work on the prefrontal cortex. In Schizophrenia: Scientific Progress, (ed. Schulz, S. C. and Tamminga, C. A.), pp. 227–246. Oxford University Press: New YorkGoogle Scholar
Goldberg, T. E., Weinberger, D. R., Pliskin, N. H., Berman, K. B. & Podd, M. H. (1989). Recall memory deficit in schizophrenia. Schizophrenia Research 2, 251–257.CrossRefGoogle ScholarPubMed
Goldberg, T. E., Ragland, J. D., Torrey, E. F., Bigelow, L. B., Gold, J. M. & Weinberger, D. R. (1990 a). Neuropsychological assessment of monozygotic twins discordant for schizophrenia. Archives of General Psychiatry 47, 1066–1072.CrossRefGoogle ScholarPubMed
Goldberg, T. E., Saint-Cyr, J. A. & Weinberger, D. R. (1990 b). Assessment of procedural learning and problem solving in schizophrenic patients by Tower of Hanoi type tasks. Journal of Neuropsychiatry and Clinical Neuroscience 2, 165–174.Google Scholar
Goldberg, T. E., Greenberg, R. D., Griffin, S. J., Gold, J. M., Kleinman, J. E., Pickar, D., Schultz, S. C. & Weinberger, D. R. (1992). The impact of clozapine on cognition and psychiatric symptoms in patients with schizophrenia. British Journal of Psychiatry (in the press).Google Scholar
Goldman-Rackic, P. S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational knowledge. In Handbook of Physiology, Vol. 5 (ed. Plum, F. and Mountcastle, V.), (pp. 373–417. American Physiology Society, Washington, D.C.Google Scholar
Gottesman, I. I. & Shields, J. A. (1972). Schizophrenia and Genetics: A Twin Study Vantage Point. Academic Press: New York.Google Scholar
Gruzelier, J., Seymour, K., Wilson, L., Jolley, A. & Hirsch, S. (1988). Impairments on neuropsychologic tests of temporohippocampal and frontohippocampal functions and word fluency in remitting schizophrenia and affective disorders. Archives of General Psychiatry 45, 623–629.CrossRefGoogle ScholarPubMed
Heindel, W. C., Salmon, D. P. & Butters, N. (1992). Neuropsychological differentiation of memory impairments. In Memory and Aging (ed. Gilmore, G., Whitehouse, P., & Wyke, M.). Springer: New York.Google Scholar
Helkala, E-L., Laurlumma, V., Soininen, H. & Riekkinen, P. J. (1988). Recall and recognition memory in patients with Alzheimer's and Parkinson's diseases. Annals of Neurology 24, 214–217.CrossRefGoogle ScholarPubMed
Hitch, G. (1984). Working memory. Psychological Medicine 14, 265–271.CrossRefGoogle ScholarPubMed
Hollingshead, A. G. & Redlich, F. C. (1958). Social Class and Mental Illness. John Wiley: New York.CrossRefGoogle Scholar
Holzman, P. S., Kringlen, E., Lery, D. L. & Haberman, S. (1980). Deviant eye tracking in twins discordant for schizophrenia: A replication. Archives of General Psychiatry 37, 627–631.CrossRefGoogle ScholarPubMed
Huberty, C. J. & Morris, J. D. (1989). Multivariate analysis versus multiple univariate analyses. Psychological Bulletin 105, 302–308.CrossRefGoogle Scholar
Huston, P. E. & Shakow, D. (1949). Learning capacity in schizophrenia. American Journal of Psychiatry 105, 881–888.CrossRefGoogle ScholarPubMed
Jakob, H. & Beckmann, H. (1986). Prenatal developmental disturbances in the limbic allocortex in schizophrenics. Journal of Neural Transmission 65, 303–326.CrossRefGoogle ScholarPubMed
Jetter, W., Poser, U., Freeman, R. B. & Markowitsch, H. J. (1986). A verbal long term memory defect in frontal lobe damaged patients. Cortex 22, 229–246.CrossRefGoogle Scholar
Kendler, K. S. & Robinette, C. D. (1983). Schizophrenia in the National Academy of Sciences-National Research Council Twin Registry: a 16-year update. American Journal of Psychiatry 140, 151–1563.Google ScholarPubMed
Killian, G. A., Holzman, P. S., Davis, J. M., & Gibbons, R. (1984). Effects of psychotropic medication on selected cognitive and perceptual measures. Journal of Abnormal Psychology 93, 58–70.CrossRefGoogle ScholarPubMed
Koh, S. D. (1978). Remembering of verbal material by Schizophrenic young adults. In Language and Cognition in Schizophrenia (ed. Schwartz, S.), pp. 555–599. Lawrence Erlbaum: Englewood Cliffs, New Jersey.Google Scholar
Koh, S. D. & Kayton, L. (1974). Memorization of ‘unrelated’ word strings by young non-psychotic schizophrenics. Journal of Abnormal Psychology 83, 14–22.CrossRefGoogle Scholar
Kolb, B. & Whishaw, I. Q. (1983). Performance of schizophrenic patients on test sensitive to left or right frontal, temporal, or parietal function in neurological patients. Journal of Nervous and Mental Disease 171, 435–443.CrossRefGoogle ScholarPubMed
Kopelman, M. D. (1986). Clinical tests of memory. British Journal of Psychiatry 148, 517–525.CrossRefGoogle ScholarPubMed
Kopelman, M. D. & Corn, T. H. (1988). Cholinergic ‘blockade’ as a model for cholinergic depletion. A comparison of the memory deficits with those of Alzheimer-type dementia and the alcoholic Korsakoff syndrome. Brain 111, 1079–1110.CrossRefGoogle Scholar
Lederlof, R., Friberg, L., Jonsson, E. & Kaij, L. (1961). Studies on similarity diagnosis in twins with the aid of a mailed questionnaire. Acta Genetica et Statistica Medica 11, 338–362.Google Scholar
McClain, L. (1983). Encoding and retrieval in schizophrenics' free recall. Journal of Nervous and Mental Disease 171, 471–479.CrossRefGoogle ScholarPubMed
McGlashan, T. H. & Williams, P. V. (1990). Predicting outcome in schizoaffective psychosis. Journal of Nervous and Mental Disease 178, 518–520.CrossRefGoogle ScholarPubMed
McKenna, P. J., Tamlyn, D., Lund, C. E., Mortimer, A. M., Hammond, S. & Baddeley, A. D. (1990). Amnesic syndrome in schizophrenia. Psychological Medicine 20, 967–972.CrossRefGoogle ScholarPubMed
Manschreck, T. C., Maher, B. A., Rosenthal, J. E. & Berner, J. (1991). Reduced primacy and related features of schizophrenia. Schizophrenia Research 5, 35–41.CrossRefGoogle ScholarPubMed
Mungas, D. (1983). Differential clinical sensitivity of specific parameters of the Rey auditory-verbal learning test. Journal of Consulting and Clinical Psychology 51, 848–855.CrossRefGoogle ScholarPubMed
Munro, A. (1982). Paranoia revisited. British Journal of Psychiatry 141, 344–349.CrossRefGoogle ScholarPubMed
Novoa, O. P. & Ardila, A. (1987). Linguistic abilities in patients with prefrontal damage. Brain and Language 30, 206–225.CrossRefGoogle ScholarPubMed
Opjordsmoen, S. (1989). Delusional disorders. I. comparative long-term outcome. Acta Psychiatrica Scandinavica 80, 603–612.CrossRefGoogle ScholarPubMed
Perlick, D., Stanstny, P., Katz, I., Mayer, M. & Mattis, S. (1986). Memory deficits and anticholinergic levels in chronic schizophrenia. American Journal of Psychiatry 143, 230–232.Google ScholarPubMed
Plomin, R. (1990). The role of inheritance in behavior. Science 248, 183–188.CrossRefGoogle ScholarPubMed
Reveley, A. M., Reveley, M. A., Clifford, C. A. & Murray, R. M. (1982). Cerebral ventricular size in twins discordant for schizophrenia. Lancet i, 540–541.CrossRefGoogle Scholar
Russell, E. W. (1975). A multiple scoring method of the assessment of complex memory functions. Journal of Consulting and Clinical Psychology 43, 800–809.CrossRefGoogle Scholar
Saint-Cyr, J. A., Taylor, A. E. & Lang, A. E. (1988). Procedural learning and neostriatal dysfunction in man. Brain 109, 845–883.Google Scholar
Sattler, J. M. & Nordmark, J. T. (1971). Verbal learning in schizophrenics and normals. Psychological Record 21, 241–246.CrossRefGoogle Scholar
Saykin, A. J., Gur, R. C., Gur, R. E., Mozley, P. D., Mozley, L. H., Resnick, S. M., Kester, D. B. & Stafiniak, P. (1991). Neuropsychological function in schizophrenia: selective impairment in memory and learning. Archives of General 48, 618–624.CrossRefGoogle ScholarPubMed
Sengel, R. A. & Lovalla, W. R. (1983). Effects of cueing on immediate and recent memory in schizophrenics. Journal of Nervous and Mental Disease 171, 426–430.CrossRefGoogle ScholarPubMed
Shakow, D. (1981). The place of cooperation in the examination of mental disorder. Journal of Nervous and Mental Disorders 169, 127–137.CrossRefGoogle ScholarPubMed
Silverstein, A. B. (1985). Two and four subtest short forms of the WAIS-R: A close look at validity and reliability. Journal of Clinical Psychiatry 41, 95–97.Google Scholar
Snyder, S., Greenberg, D. & Yamamura, H. I. (1974). Anti-schizophrenic drugs and brain cholinergic receptors. Affinity for muscarinic sites predicts extrapyramidal effects. Archives of General Psychiatry 31, 58–61.CrossRefGoogle Scholar
Snyder, S. H. & Yamamura, H. I. (1977). Antidepressants and the muscarinic acetylcholine receptor. Archives of General Psychiatry 34, 236–239.CrossRefGoogle ScholarPubMed
Spitzer, R. L., Gibbon, M. & Endicott, J. (1979). Global Assessment Scale. New York State Psychiatric Institute: New York.Google Scholar
Spitzer, R. L., Williams, J. B., Gibbon, M. & First, M. B. (1988). Structured Clinical Interview for DSM-III-R, New York State Psychiatric Institute: New York.Google Scholar
Spohn, H., Lacoursiere, R., Thompson, K. & Coyne, L. (1977). Phenothiazine effects on psychological and psychophysiological dysfunction in chronic schizophrenics. Archives of General Psychiatry 34, 633–644.CrossRefGoogle ScholarPubMed
Suddath, R. L., Christison, G. W., Torrey, E. F., Casanova, M. F. & Weinberger, D. R. (1990). Anatomical abnormalities in the brain of monozygotic twins discordant for schizophrenia. New England Journal of Medicine 322, 789–794.CrossRefGoogle ScholarPubMed
Torrey, E. F. (1988). Surviving Schizophrenia. Harper & Row: New York.Google Scholar
Traupmann, K. L. (1980). Encoding processes and memory for categorically related word by schizophrenic patients. Journal of Abnormal Psychology 89, 704–716.CrossRefGoogle Scholar
Tulving, E. (1983). Elements of Episodic Memory. Oxford University Press: New York.Google Scholar
Tune, L. E., Strauss, M. E., Lew, M. F., Breitlinger, E. & Coyle, J. T. (1982). Serum levels of anticholinergic drugs and impaired recent memory in chronic schizophrenic patients. American Journal of Psychiatry 139, 1460–1462.Google ScholarPubMed
Warrington, E. K. (1988). Recognition Memory Test. Psychological Assessment Resources: Odessa, FL.Google Scholar
Watkins, M. J. (1990). Mediationism and the obfuscation of memory. American Psychologist 45, 328–335.CrossRefGoogle ScholarPubMed
Wechsler, D. (1981). WAIS-R. The Psychological Corporation: New York.Google Scholar
Wechsler, D. & Stone, L. P. (1985). The Wechsler Memory Scale. The Psychological Corporation: New York.Google Scholar
Weinberger, D. R. (1991). Anteromedial temporal-prefrontal connectivity: a functional neuroanatomical system implicated in schizophrenia. In Psychopathology and the Brain (ed. Carroll, B.), pp. 25–43. Raven Press: New York.Google Scholar
Weinberger, D. R., DeLisi, L. E., Neophytides, A. N. & Wyatt, R. J. (1981). Familial aspects of CT scan abnormalities in chronic schizophrenia patients. Psychiatry Research 4, 65–71.CrossRefGoogle Scholar
Weinberger, D. R., Berman, K. F. & Zee, R. F. (1986). Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia: I. Regional cerebral blood flow evidence. Archives of General Psychiatry 43, 114–124.CrossRefGoogle ScholarPubMed
Weinberger, D. R., Berman, K. F. & Illowsky, B. P. (1988). Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia: III. A new cohort and evidence for a monoaminergic mechanism. Archives of General Psychiatry 45, 609–615.CrossRefGoogle Scholar
Wilson, R. S. (1980). Blood typing and twin zygosity. Acta Medic Genetica 29, 103–126.Google ScholarPubMed