Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-22T13:56:57.018Z Has data issue: false hasContentIssue false
  • English
  • Français

Schizophrenia and the normal functional development of the prefrontal cortex

Published online by Cambridge University Press:  31 October 2008

Nancy A. Breslin  and
Daniel R. Weinberger
Nancy A. Breslin
Affiliation:
Clinical Brain Disorders Branch, National Institutes of Mental HealthIntramural Research Program
Daniel R. Weinberger
Affiliation:
Clinical Brain Disorders Branch, National Institutes of Mental HealthIntramural Research Program
Get access Rights & Permissions [Opens in a new window]

Abstract

Schizophrenia is being increasingly viewed as a neurodevelopmental disorder, that is, one in which early, fixed pathology becomes manifest clinically during the normal course of maturation of the brain. Evidence for this position comes first from neuroimaging research, such as (1) studies that demonstrate morphologic brain changes (such as ventriculomegaly on CT scans) even in first break patients; and (2) a lack of correlation between these morphologic changes and duration of illness. Another source of evidence is studies of normal brain development in rodents and primates, including research that shows (1) the prefrontal cortex is a late maturing part of the brain, and (2) lesions of the prefrontal cortex may be initially silent and show delayed onset of dysfunction as the brain matures. A neurodevelopmental approach to schizophrenia, in turn, has stimulated further work into the normal development of brain regions implicated in the illness, such as the frontal cortex. Thus, the fields of neuropsychiatry and neurodevelopment have been mutually stimulated during the course of this work. In addition, viewing schizophrenia in developmental terms may have implications for the understanding of changes in cognition and behavior during normal adolescence.

Type
Research Article
Information
Development and Psychopathology , Volume 2 , Issue 4 , October 1990 , pp. 409 - 424
Copyright
Copyright © Cambridge University Press 1990

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

Alexander, G. E., & Goldman, P. S. (1978). Functional development of the dorsolateral prefrontal cortex: An analysis utilizing reversible cryogenic depression. Brain Research, 143, 233–249.CrossRefGoogle Scholar
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1985). Catecholamines and cognitive decline in aged non-human primates. In Olton, D. S., Gamzu, E., & Corkin, S. (Eds.), Annals of the New York Academy of Sciences (pp. 218–234). New York: New York Academy of Sciences.Google Scholar
Belmaker, R., Pollin, W., Wyatt, R. J., & Cohen, S. (1974). A follow-up of monozygotic twins discordant for schizophrenia. Archives of General Psychiatry, 30, 219–.CrossRefGoogle ScholarPubMed
Benes, F. M. (1989). Myelination of cortical-hippo-campal relays during late adolescence. Schizophrenia Bulletin, 15, 585–593.CrossRefGoogle ScholarPubMed
Benes, F. M., Davidson, J., & Bird, E. D. (1986). Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Archives of General Psychiatry, 43, 31–35.CrossRefGoogle ScholarPubMed
Berry, M. (1974). Development of the cerebral neocortex in the rat. In Gottlieb, G. (Ed.), Studies on the development of behavior and the nervous system: Aspects of neurogenesis (pp. 8–67). New York: Academic Press.Google Scholar
Bogerts, B. (1989). The role of limbic and paralimbic pathology in the etiology of schizophrenia. Psychiatry Research, 29, 255–256.CrossRefGoogle ScholarPubMed
Bogerts, B., Ashtari, M., Degreet, G., Alvir, J. M., Bilder, R. M., & Lieberman, J. A. (1990). Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia. Psychiatry Research: Neuroimaging, 35, 1–13.CrossRefGoogle ScholarPubMed
Bogerts, B., Meertz, E., Schonfeldt-Bausch, R. (1985). Basal ganglia and limbic system pathology in schizophrenia: A morphometeric study. Archives of General Psychiatry, 42, 784–791.CrossRefGoogle Scholar
Breslin, N. A., Daniel, D. G., Gold, J. M., Kola-chana, B. S., Kleinman, J. E., & Weinberger, D. R. (1990). Effects of SKF-38393 (D1 agonist) on schizophrenia. APA 143rd Annual Meeting New Research Program and Abstracts (NR124).Google Scholar
Breslin, N. A., & Weinberger, D. R. (in press). Neuro-developmental implications of findings from brain imaging studies of schizophrenia. In Mednick, S. A., Cannon, T. D., Barr, C. E., & Lyon, M. (Eds.), Fetal neurodevelopment and adult schizophrenia. New York: Cambridge University Press.Google Scholar
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
Brozowski, T. J., Brown, R. M., Rosvold, H. E., & Goldman, P. S. (1979). Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science, 205, 929–932.CrossRefGoogle Scholar
Ciompi, L. (1985). Aging and schizophrenic psychosis. Acta Psychiatrica Scandinavica, 71(Suppl. 319), 93–105.CrossRefGoogle Scholar
Cortés, R., Gueye, B., Pazos, A., Probst, A., & Palacios, J. M. (1989). Dopamine receptors in human brain: Autoradiographic distribution of D1 sites. Neuroscience, 28, 263–272.CrossRefGoogle ScholarPubMed
Council on Scientific Affairs (1988). Positron emission tomography – a new approach to brain chemistry. JAMA, 260, 2704–2710.CrossRefGoogle Scholar
Creese, I., Burt, D. R., & Snyder, S. H. (1976). Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science, 192, 481–483.CrossRefGoogle ScholarPubMed
Crow, T. J. (1982). Two syndromes in schizophrenia? Trends in Neurosciences, 10, 351–354.CrossRefGoogle Scholar
Daniel, D. G., Breslin, N. A., Clardy, J., Gold, J. M., Kleinman, J. E., & Weinberger, D. R. (1990). A trial of L-Dopa and molindone in schizophrenia. APA 143rd Annual Meeting New Research Program and Abstracts(NR136).Google Scholar
Daniel, D. G., & Weinberger, D. R. (1991). Ex multi uno: A case for neurobiological homogeneity in schizophrenia. In Tamminga, C. A. & Schulz, S. C. (Eds.), Advances in neuropsychiatry and psycho-pharmacology (pp. 227–235). New York: Raven.Google Scholar
Davison, K., & Bagley, C. R. (1969). Schizophrenia-like psychoses associated with organic disorders of the central nervous system. British Journal of Psychiatry, 113(Suppl. 1), 18–69.Google Scholar
DeLisi, L. E., Schwartz, C. C., Targum, S. D., Byrnes, S. M., Cannon-Spoor, E., Weinberger, D. R., & Wyatt, R. J. (1983). Ventricular brain enlargement and outcome of acute schizophreni-form disorder. Psychiatry Research, 9, 169–171.CrossRefGoogle Scholar
Diamond, A., & Goldman-Rakic, P. S. (1989). Comparison of human infants and rhesus monkeys on Piaget's A not B task: Evidence for dependence on dorsolateral prefrontal cortex. Experimental Brain Research, 74, 24–40.CrossRefGoogle Scholar
Diamond, A., Zola-Morgan, S., & Squire, L. R. (1989). Successful performance by monkeys with lesions of the hippocampal formation on A not B and object retrieval, two tasks that mark developmental changes in human infants. Behavioral Neuroscience, 103, 526–537.CrossRefGoogle Scholar
Fallen, J. H. (1988). Topographic organization of ascending dopaminergic projections. In Kalivas, P. W. & Nemeroff, C. B. (Eds.), Annals of the New York Academy of Sciences: The mesocortical dopamine system (pp. 1–9). New York: New York Academy of Sciences.Google Scholar
Falloon, I. R. H., Boyd, J. L., McGill, C. W., Razani, J., Moss, H. B., & Gilderman, A. M. (1982). Family management in the prevention of exacerbations of schizophrenia. New England Journal of Medicine, 306, 1437–1440.CrossRefGoogle ScholarPubMed
Feinberg, I. (1982–1983). Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? Journal of Psychiatric Research, 17, 319–334.CrossRefGoogle ScholarPubMed
Fibiger, H. C., & Phillips, A. G. (1988). Mesocorticolimbic dopamine systems and reward. Annals of theNew York Academy of Sciences, 537, 206–215.CrossRefGoogle ScholarPubMed
Fuster, J. M. (1989). The prefrontal cortex. New York: Raven.Google Scholar
Gilmore, D. P., & Wilson, C. A. (1983). Indoleamine and catecholamine concentrations in the mid-term human fetal brain. Brain Research Bulletin, 10, 395–398.CrossRefGoogle ScholarPubMed
Golden, C. J., Moses, J. A., Zelazowski, R., Braber, B., Zatz, L. M., Horvath, T. B., & Berger, P. A. (1980). Cerebral ventricular size and neuropsychological impairment in young chronic schizophrenics. Archives of General Psychiatry, 37, 619–623.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P. S. (1987). Development of cortical circuitry and cognitive function. Child Development, 58, 601–622.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P. S., & Brown, R. M. (1982). Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. Developmental Brain Research, 4, 339–349.CrossRefGoogle Scholar
Goldman-Rakic, P. S., Selemon, L. D., & Schwartz, M. L. (1984). Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience, 12, 719–743.CrossRefGoogle ScholarPubMed
Green, M. F., Satz, P., Soper, H. V., & Kharabi, F. (1987). Relationship between physical anomalies and age at onsets of schizophrenia. American Journal of Psychiatry, 144, 666–667.Google ScholarPubMed
Haug, J. O. (1962). Pneumoencephalographic studies in mental disease. Acta Psychiatrica Scandinavica, 38(Suppl.), 11–104.Google ScholarPubMed
Heller, A., Hoffmann, P. C., Kotake, C., & Shalaby, l. (1983). Regulation of the morphologic and biochemical differentiation of embryonic dopamine neurons in vitro. Psychopharmacology Bulletin, 19, 311–316.Google Scholar
Huttenlocher, R. P. (1979). Synaptic density in human frontal cortex – developmental changes and effects of aging. Brain Research, 163, 195–205.Google ScholarPubMed
Illowsky, B. P., Juliano, D. M., Bigelow, L. B., & Weinberger, D. R. (1988). Stability of CT scan findings in schizophrenia: Results of an eight year follow-up study. Journal of Neurology, Neurosurgery and Psychiatry, 51, 209–213.Google Scholar
Jakob, H., & Beckmann, H. (1986). Prenatal development disturbances in the limbic allocortex in schizophrenics. Journal of Neural Transmission, 65, 303–326.CrossRefGoogle ScholarPubMed
Jaskiw, G. E., Andreasen, N. C., & Weinberger, D. R. (1987). X-ray computed tomography and magnetic resonance imaging in psychiatry. In Hales, R. E. & Frances, A. I. (Eds.), Psychiatry update (pp. 260–299). Washington: American Psychiatric Press, Inc.Google Scholar
Jaskiw, G. E., Karoum, F., & Weinberger, D. R. (1990). Persistent elevations of dopamine and metabolites in nucleus accumbens after mild subchronic stress in rats with ibotinic acid lesions of medical prefrontal cortex. Brain Research, 534, 321–323.CrossRefGoogle Scholar
Jeste, D. V., & Lohr, J. B. (1989). Hippocampal pathologic findings in schizophrenia. Archives of General Psychiatry, 46, 1019–1024.CrossRefGoogle ScholarPubMed
Kalsbeek, A. (1989). The role of dopamine in the development of the rat prefrontal cortex. Amsterdam: Krips Repro Meppel. (Academisch Proefschcrift)Google Scholar
Kalsbeek, A., Buijs, R. M., Hofman, M. A., Matthijssen, M. A. H., Pool, C. W., & Uylings, H. B. M. (1987). Effects of neonatal thermal lesioning of the mesocortical dopaminergic projection on the development of the rat prefrontal cortex. Developmental Brain Research, 32, 1987.CrossRefGoogle Scholar
Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., & Uylings, H. B. M. (1988). Development of the dopaminergic innervation in the prefrontal cortex of the rat. Journal of Comparative Neurology, 269, 58–72.CrossRefGoogle ScholarPubMed
Kelsoe, J. R., Cadet, J. L., Pickar, D., & Weinberger, D. R. (1988). Quantitative neuroanatomy in schizophrenia. Archives of General Psychiatry, 45, 533–541.CrossRefGoogle ScholarPubMed
Kendler, K. S., Tsuang, M. T., & Hays, P. (1987). Age at onset in schizophrenia: A family perspective. Archives of General Psychiatry, 44, 881–890.CrossRefGoogle Scholar
Kirch, D. G., & Weinberger, D. R. (1986). Anatomical neuropathology in schizophrenia: post-mortem findings. In Nasrallah, H. A. & Weinberger, D. R. (Eds.), Handbook of schizophrenia, vol. 1: The neurology of schizophrenia (pp. 325–348). Amsterdam: Elsevier.Google Scholar
Kolb, B., & Nonneman, A. J. (1976). Functional development of prefrontal cortex in rats continues into adolescence. Science, 193, 335–336.CrossRefGoogle ScholarPubMed
Kolb, B., & Whishaw, I. Q. (1989). Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Progress in Neurobiology, 32, 235–276.CrossRefGoogle ScholarPubMed
Kostovic, I., Skavic, J., & Strinovic, D. (1988). Acetylcholinesterase in the human frontal associative cortex during the period of cognitive development: Early laminar shifts and late innervation of pyramidal neurons. Neuroscience Letters, 90, 107–112.CrossRefGoogle ScholarPubMed
Lewis, D. A. (1990). The dopaminergic innervation of human prefrontal cortex. Biological Psychiatry (Abstracts), 27, 140A.Google Scholar
Mahut, H., & Moss, M. (1986). The monkey and the sea horse. In Isaacson, R. L. & Pribram, K. H. (Eds.), The hippocampus (pp. 241–279). New York: Plenum.CrossRefGoogle Scholar
Meltzer, H. Y. (1987). Biological studies in schizophrenia. Schizophrenia Bulletin, 13, 77–111.CrossRefGoogle ScholarPubMed
Nasrallah, H. A., Andreasen, N. C., Coffman, J. A., Olson, S. C., Dunn, V. D., Ehrhardt, J. C., & Chapman, S. M. (1986). A controlled magnetic resonance imaging study of corpus callosum thickness in schizophrenia. Biological Psychiatry, 21, 274–282.CrossRefGoogle ScholarPubMed
Nasrallah, H. A., Kuperman, S., Hamra, B. J., & McCalley-Whitters, M. (1983). Clinical differences between schizophrenic patients with and without large cerebral ventricles. Journal of Clinical Psychiatry, 44, 407–409.Google ScholarPubMed
Pearlson, G. D., Garbacz, D. J., Moberg, P. J., Ahn, H. S., & DePaulo, J. R. (1985). Symptomatic, familial, perinatal, and social correlates of computerized axial tomography (CAT) changes in schizophrenics and bipolars. Journal of Nervous and Mental Disease, 173, 42–50.CrossRefGoogle ScholarPubMed
Peroutka, S. J., & Snyder, S. H. (1980). Relationship of neuroleptic drug effects at brain dopamine, serotonin, alpha-adrenergic, and histamine receptors to clinical potency. American Journal of Psychiatry, 137, 1518–1522.Google ScholarPubMed
Pycock, C. J., Kerwin, R. W., & Carter, C. J. (1980). Effect of lesion of cortical dopamine terminals on subcortical dopamine receptors in rats. Nature, 286, 74–77.CrossRefGoogle ScholarPubMed
Rakic, P. (1988). Specification of cerebral cortical areas. Science, 241, 170–176.CrossRefGoogle ScholarPubMed
Rinne, J. P., Rummukainen, J., Paljarvi, L., & Rinne, U. K. (1989). Dementia in Parkinson's disease is related to neuronal loss in the medial substantia nigra. Annals of Neurology, 26, 47–50.CrossRefGoogle ScholarPubMed
Schmidt, R. H., Bjorklund, A., Lindvall, O., & Loren, 1. (1982). Prefrontal cortex: Dense dopaminergic input in the newborn rat. Developmental Brain Research, 5, 222–228.CrossRefGoogle Scholar
Schulz, S. C., Roller, M. M., Kishore, P. R., Hamer, R. M., Gehl, J. J., & Friedel, R. O. (1983). Ventricular enlargement in teenage patients with schizophrenia spectrum disorder. American Journal of Psychiatry, 140, 1592–1595.Google ScholarPubMed
Shelton, R. C., Karson, C. N., Doran, A. R., Pickar, D., Bigelow, L. B., & Weinberger, D. R. (1988). Cerebral structural pathology in schizophrenia: Evidence for a selective prefrontal cortical defect. American Journal of Psychiatry, 145, 154–163.Google ScholarPubMed
Siesjo, B. K., & Blennow, G. (1980). The effects of hypoxia, hypoglycemia, and epileptic seizures on brain development. In DiBenedetta, C., Balazs, R., Combos, G., & Porcellati, G. (Eds.), Multidisciptinary approach to brain development (pp. 241–252). Amsterdam: Elsevier/North-Holland.Google Scholar
Stevens, J. R. (1988). Epilepsy, psychosis and schizophrenia. Schizophrenia Research, 1, 79–89.CrossRefGoogle ScholarPubMed
Storey, P. B. (1966). Lumbar air encephalography in chronic schizophrenia: A controlled experiment. British Journal of Psychiatry, 112, 135–144.CrossRefGoogle ScholarPubMed
Suddath, R. L., Casanova, M. F., Goldberg, T. E., Daniel, D. G., Kelsoe, J. R., & Weinberger, D. R. (1989). Temporal lobe pathology in schizophrenia: A quantitative magnetic resonance imaging study. American Journal of Psychiatry, 146, 464–472.Google ScholarPubMed
Suddath, R. L., Christison, G. W., Torrey, E. F., Casanova, M. F., & Weinberger, D. R. (1990). Cerebral anatomical abnormalities in monozygotic twins discordant for schizophrenia. New England Journal of Medicine, 322, 789–794.CrossRefGoogle ScholarPubMed
Takahashi, R., Inaba, Y., Inanaga, K., Kato, N., Kumashiro, H., Nishimura, T., Okuma, T., Otsuki, S., Sakai, T., Sato, T., & Shimazono, Y. (1981). CT scanning and the investigation of schizophrenia. In Perris, C., Struve, G., & Jansson, B. (Eds.), Biological psychiatry 1981 (pp. 259–268). Amsterdam: Elsevier/North-Holland.Google Scholar
Tucker, T. J., & Kling, A. (1967). Differential effects of early and late lesions of frontal granular cortex in the monkey. Brain Research, 5, 377–389.CrossRefGoogle Scholar
Turner, S. W., Toone, B. K., & Brett-Jones, J. R. (1986). Computerized tomographic scan changes in early schizophrenia-preliminary findings. Psychological Medicine, 16, 219–225.CrossRefGoogle ScholarPubMed
VanEden, C. G., & Uylings, H. B. M. (1985a). Cytoarchitectonic development of the prefrontal cortex in the rat. The Journal of Comparative Neurology, 241, 253–267.CrossRefGoogle Scholar
VanEden, C. G., & Uylings, H. B. M. (1985b). Postnatal volumetric development of the prefrontal cortex in the rat. The Journal of Comparative Neurology, 241, 268–274.CrossRefGoogle Scholar
Verney, C., Berger, B., Adrien, J., Vigny, A., & Gay, M. (1982). Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using antityrosine hydroxylase antibodies. Developmental Brain Research, 5, 41–52.CrossRefGoogle Scholar
Vita, A., Sacchetti, E., Valvassori, G., & Cazzullo, C. L. (1988). Brain morphology in schizophrenia: A 2-to 5-year CT scan follow-up study. Acta Psychiatrica Scandinavica, 78, 618–621.CrossRefGoogle ScholarPubMed
Weinberger, D. R. (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry, 44, 660–669.CrossRefGoogle ScholarPubMed
Weinberger, D. R. (1988). Premorbid neuropathology in schizophrenia. Lancet, ii, 445.CrossRefGoogle Scholar
Weinberger, D. R., Berman, K. F., & Chase, T. N. (1988). Mesocortical dopaminergic function and human cognition. In Kalivas, P. W. & Nemeroff, C. B. (Eds.), Annals of the New York Academy of Sciences: The mesocortical dopamine system (pp. 330–338). New York: The New York Academy of Sciences.Google Scholar
Weinberger, D. R., Berman, K. F., & Zec, R. F. (1986). Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenic: I. Regional blood flow evidence. Archives of General Psychiatry, 43, 114–124.CrossRefGoogle ScholarPubMed
Weinberger, D. R., Cannon-Spoor, E., Potkin, S. G., & Wyatt, R. J. (1980). Poor premorbid adjustment and CT scan abnormalities in chronic schizophrenia. American Journal of Psychiatry, 137, 1410–1413.Google ScholarPubMed
Weinberger, D. R., DeLisi, L. E., Perman, G. P., Targum, S., & Wyatt, R. J. (1982). Computed tomography in schizophreniform disorder and other acute psychiatric disorders. Archives of General Psychiatry, 39, 778–783.CrossRefGoogle ScholarPubMed
Weinberger, D. R., Torrey, E. F., Neophytides, A. N., & Wyatt, R. J. (1979). Lateral cerebral ventricular enlargement in chronic schizophrenia. Archives of General Psychiatry, 36, 735–739.CrossRefGoogle ScholarPubMed
White, N. M. (1989). Reward or reinforcement: what's the difference? Neuroscience and Biobehavioral Reviews, 13, 181–186.CrossRefGoogle ScholarPubMed
Williams, A. O., Reveley, M. A., Kolakowska, T., Ardern, M., & Mandelbrote, B. M. (1985). Schizophrenia with good and poor outcome II: Cerebral ventricular size and its clinical significance. British Journal of Psychiatry, 146, 239–246.CrossRefGoogle ScholarPubMed
Yakovlev, P. I., & LeCours, A.-R. (1964). The myelogenetic cycles of regional maturation of the brain. In Minkowski, A. (Ed.), Regional development of the brain in early life (pp. 3–70). Boston: Black-well.Google Scholar