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Developmental changes in stress adaptation in relation to psychopathology

Published online by Cambridge University Press:  31 October 2008

Francine M. Benes
Francine M. Benes*
Affiliation:
Laboratory for Structural Neuroscience, McLean Hospital, Harvard Medical School
*
Address correspondence and reprint requests to: Francine M. Benes, Laboratory for Structural Neuroscience, McLean Hospital, 115 Mill Street, Belmont, MA 02178.
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Abstract

As modern neuroscience seeks to understand the neural bases for mental illness, it is becoming increasingly important to define how and when complex neural circuits may be altered in individuals who carry the genetic vulnerability for psychopathology. One factor that could potentially play a contributory role in mental illness is the stress response. A variety of studies suggest that stress can alter the activity of several key cortical neurotransmitters, including glutamate, γ-aminobutyric acid, dopamine, and serotonin. Specifically, exposure to neurotoxic levels of adrenal steroid hormone, particularly if this occurs early in life, could potentially induce permanent changes of these transmitter systems in corticolimbic regions, such as the hippocampal formation and cingulate gyrus, that have a high density of glucocorticoid receptors. Overall, exposure to severe stress during the perinatal period could potentially induce alterations in the circuitry of the anterior cingulate cortex and hippocampal formation and interfere with the normal mechanisms underlying attention and learning.

Type
Articles
Information
Development and Psychopathology , Volume 6 , Issue 4 , Fall 1994 , pp. 723 - 739
Copyright
Copyright © Cambridge University Press 1994

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References

Abarca, J., & Bustos, G. (1985). Release of D-[3-H]aspartic acid from the rat substantia nigra: Effect of veratridine-evoked depolarization and cortical ablation. Neurochemistry, 7, 229–236.CrossRefGoogle ScholarPubMed
Akbarian, S., Bunney, W. E., Potkin, S. G., Wigal, S. B., Hagman, J. D., Sandman, C. A., & Jones, E. G. (1993). Altered distribution of nicotinamideadenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Archives of General Psychiatry, 50, 227–230.Google ScholarPubMed
American Psychiatric Association. (1980). Diagnostic and statistical manual of mental disorders (3rd ed.). Washington, DC: Author.Google Scholar
Angevine, J. B. (1965). Time of neuron origin in the hippocampal region: An autoradiographic study in the mouse. Experimental Neurology, 13, 1–70.Google Scholar
Antelman, S., Knopf, S., Caggiula, A., Kocan, D., Lysle, D., & Edwards, D. (1988). Stress and enhanced dopamine utilization in the frontal cortex: The myth and the reality. Annals of the New York Academy of Sciences, 537, 262–272.CrossRefGoogle ScholarPubMed
Ardeleanu, A., & Sterescu, N. (1978). RNA and DNA synthesis in developing rat brain: Hormonal influences. Psychoneuroendocrinology, 3, 93–101.CrossRefGoogle ScholarPubMed
Armanini, M. P., Hutchins, C., Stein, B. A., & Sapolsky, R. M. (1990). Clucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Research, 532, 7–12.CrossRefGoogle Scholar
Arora, R. C., & Meltzer, H. Y. (1991). Serotonin-25-HT-2 receptor binding in the frontal cortex of schizophrenic patients. Journal of Neural Transmission, 85, 19–29.CrossRefGoogle ScholarPubMed
Artola, A., & Singer, W. (1987). Long-term potentiation and NMDA receptors in rat visual cortex. Nature (London), 330, 649–652.CrossRefGoogle ScholarPubMed
Balazs, R., & Cotterrell, M. (1972). Effect of hormonal state on cell number and functional maturation of the brain. Nature (London), 236, 348–350.CrossRefGoogle ScholarPubMed
Benes, F. M. (1993a). Neurobiological investigations in cingulate cortex of schizophrenic brain. Schizophrenia Bulletin, 19, 537–549.CrossRefGoogle ScholarPubMed
Benes, F. M. (1993b). Relationship of cingulate cortex to schizophrenia and other psychiatric disorders. In Vogt, B. A. & Gabriel, M. (Eds.), The neurobiology of cingulate cortex and limbic thalamus (pp. 581–605). Boston: Birkhauser.CrossRefGoogle Scholar
Benes, F. M. (in press). Excitotoxicity in the development of corticolimbic alterations in schizophrenic brain. Association for Research of Nervous and Mental Diseases.Google Scholar
Benes, F. M., & Bird, E. D. (1987). An analysis of the arrangement of neurons in the cingulate cortex of schizophrenic patients. Archives of General Psychiatry, 44, 608–616.CrossRefGoogle ScholarPubMed
Benes, F. M., Davidson, J., & Bird, E. D. (1986). Quantitative cytoarchitectural studies of cerebral cortex of schizophrenics. Archives of General Psychiatry, 43, 31–35.CrossRefGoogle ScholarPubMed
Benes, F. M., Majocha, R., Bird, E. D., & Marrotta, C. A. (1987). Increased vertical axon numbers in cingulate cortex of schizophrenics. Archives of General Psychiatry, 44, 1017–1021.CrossRefGoogle ScholarPubMed
Benes, F. M., McSparren, J., Bird, E. D., Vincent, S. L., & SanGiovanni, J. P. (1991). Deficits in small interneurons in prefrontal and anterior cingulate cortex of schizophrenia and schizoaffective patients. Archives of General Psychiatry, 48, 996–1001.CrossRefGoogle ScholarPubMed
Benes, F. M., Sorensen, I., & Bird, E. D. (1991). Morphometric analyses of the hippocampal formation in schizophrenic brain. Schizophrenia Bulletin, 17, 597–608.CrossRefGoogle Scholar
Benes, F. M., Sorensen, I., Vincent, S. L., Bird, E. D., & Sathi, M. (1992). Increased density of glutamateimmunoreactive vertical processes in superficial laminae in cingulate cortex of schizophrenic brain. Cerebral Cortex, 2, 502–512.CrossRefGoogle ScholarPubMed
Benes, F. M., Vincent, S. L., Alsterberg, G., Bird, E. D., & SanGiovanni, J. P. (1992). Increased GABA-A receptor binding in superficial layers of cingulate cortex in schizophrenics. Journal of Neuroscience, 12, 924–929.CrossRefGoogle ScholarPubMed
Benes, F. M., Vincent, S. L., & Molloy, R. (1993). Dopamine-immunoreactive axon varicosities form non-random contacts with GABA-immunoreactive neurons in rat and medial prefrontal cortex. Synapse, 15, 285–295.CrossRefGoogle Scholar
Bennett, J. P., Enna, S. J., Bylund, D. B., Gillin, J. C., Wyatt, R. J., & Synder, S. H. (1979). Neurotransmitter receptors in frontal cortex of schizophrenics. Archives of General Psychiatry, 36, 927–934.CrossRefGoogle ScholarPubMed
Benowitz, L., & Routtenberg, A. (1987). A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism and synaptic plasticity. Trends in Neuroscience, 10, 527–532.CrossRefGoogle Scholar
Berger, B., & Verney, C. (1984). Development of the catecholamine innervation in rat neocortex. Morphological features. In Descarries, L., Reader, T. R., & Jasper, H. H. (Eds.), Monoamine innervation of cerebral cortex (pp. 95–121). New York: Liss.Google Scholar
Bliss, R., & Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path. Journal of Physiology, 232, 331–356.CrossRefGoogle Scholar
Boadle-Biber, M., Corley, K., Graves, L., Phan, T., & Rosecrans, J. (1989). Increase in the activity of tryptophan hydroxylase from cortex and midbrain of male Fisher 344 rats in response to acute or repeated sound stress. Brain Research, 482, 306–316.CrossRefGoogle ScholarPubMed
Bodkin, J. A. (1990). Emerging uses in high-potency benzodiazepines in psychotic disorders. Clinical Psychiatry, 51, 41–46.Google ScholarPubMed
Bogerts, B., Meertz, E., & Schonfeldt-Bausch, R. (1985). Basal ganglia and limbic system pathology in schizophrenia: A morphometric study of brain volume and shrinkage. Archives of General Psychiatry, 42, 784–791.CrossRefGoogle ScholarPubMed
Bruinink, A., Lichtensteiner, W., & Schlumpf, M. (1983). Pre- and postnatal ontogeny and characterization of dopaminergic D2, serotonergic S2, and spirodecanone binding sites in rat forebrain. Journal of Neurochemistry, 40, 1227–1237.CrossRefGoogle ScholarPubMed
Candy, J. M., & Martin, I. L. (1979). The postnatal development of the benzodiazepine receptor in the cerebral cortex and cerebellum of the rat. Journal of Neurochemistry, 32, 655–658.CrossRefGoogle ScholarPubMed
Chalmers, D. T., Kwak, S., Mansour, A., Akil, H., & Watson, S. (1993). Corticosteroids regulate brain hippocampal 5-HT1A receptor mRNA expression. Journal of Neuroscience, 13, 914–923.CrossRefGoogle ScholarPubMed
Collingridge, G., Kehl, S., & McLennan, H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. Journal of Physiology, 334, 33–46.CrossRefGoogle ScholarPubMed
Conti, F., Fabri, M., & Manzoni, T. (1988). Gluta-mate-positive cortico-cortical neurons in the somatic sensory areas I and II of cats. Journal of Neuroscience, 8, 2948–2960.CrossRefGoogle Scholar
Corda, M. G., & Biggio, G. (1986). Stress and GABAergic transmission: Biochemical and behavioural studies. In Biggio, G. & Costa, E. (Eds.), GABAergic transmission and anxiety (pp. 121–135). New York: Raven Press.Google Scholar
Cotterrell, M., Balazs, R., & Johnson, A. L. (1972). Effects of Corticosteroids on the biochemical maturation of rat brain: Postnatal cell formation. Journal of Neurochemistry, 19, 2151–2167.CrossRefGoogle ScholarPubMed
Coyle, J. T., & Enna, S. (1976). Neurochemical aspects of the ontogenesis of GABAnergic neurons in the rat brain. Brain Research, 111, 119–133.CrossRefGoogle ScholarPubMed
de Kloet, E., Rosenfeld, P., van Eekelen, J., Sutanto, W., & Levine, S. (1988). Stress, glucocorticoids and development. Progress in Brain Research, 73, 101–120.CrossRefGoogle ScholarPubMed
DeKosky, S., Scheff, S., & Cotman, C. (1984). Elevated corticosterone levels: A possible cause of reduced axon sprouting in aged animals. Neuroendocrinology, 38, 33–38.CrossRefGoogle Scholar
Deskin, R., Seidler, F. J., Whitmore, W. L., & Slotkin, T. A. (1981). Development of a noradrenergic and dopaminergic receptor system depends on maturation of their presynaptic nerve terminals in the rat brain. Journal of Neurochemistry, 36, 1683–1690.CrossRefGoogle ScholarPubMed
Deutch, A. Y., & Roth, R. H. (1990). The determinants of stress-induced activation of the prefrontal cortical dopamine system. Progressive Brain Research, 85, 367–403.CrossRefGoogle ScholarPubMed
Dunn, A. J. (1988). Stress-related activation of cerebral dopaminergic systems. Annals of the New York Academy of Sciences, 537, 188–205.CrossRefGoogle ScholarPubMed
Eccles, J. C. (1984). The cerebral neocortex. In Jones, E. G. & Peters, A. (Eds.), Cerebral cortex (Vol. 2, pp. 1–36). New York: Plenum Press.Google Scholar
Falkai, P., & Bogerts, B. (1986). Cell loss in the hippocampus of schizophrenics. European Archives of Psychiatry and Neurological Science, 236, 154–161.CrossRefGoogle ScholarPubMed
Federoff, H., Grabczyk, E., & Fishman, M. (1988). Corticosteroids suppress expression of GAP-43. Society for Neuroscience Abstracts, 14, 112.7.Google Scholar
Fride, E., Dan, Y., Feldon, H., Halvey, G., & Weinstock, M. (1986). Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiology and Behavior, 37, 681–687.CrossRefGoogle ScholarPubMed
Fuxe, K., Cintra, A., Harfstrand, A., Agnati, L. F., Kalia, M., Zoli, M., Wikstrom, A. C., Okret, S., Aronsson, M., & Gustafsson, J. A. (1987). Central glucocorticoid receptor immunoreactive neurons: New insights into the endocrine regulation of the brain. Annals of the New York Academy of Sciences, 512, 362–393.CrossRefGoogle ScholarPubMed
Gariano, R., & Groves, P. (1988). Burst firing in midbrain dopamine neurons induced by stimulation of medial prefrontal and anterior cingulate cortices. Brain Research, 462, 194–198.CrossRefGoogle ScholarPubMed
Gee, K. W., & Lan, N. C. (1991). γ-aminobutyric acid-a receptor complexes in rat frontal cortex and spinal cord show differential responses to steroid modulation. Molecular Pharmacology, 40, 995–999.Google Scholar
Gellman, R. L., & Aghajanian, G. K. (1993). Pyramidal cells in piriform context receive a convergence of inputs from monoamine activated GABAergic interneurons. Brain Research, 600, 63–73.CrossRefGoogle Scholar
Giral, P., Martin, P., Soubre, P., & Simon, P. (1988). Reversal of helpless behavior in rats by putative 5-HT1A agonists. Biological Psychiatry, 23, 237–242.CrossRefGoogle ScholarPubMed
Harrison, N. L., Dorota Majewska, M., Harrington, J. W., & Barker, J. L. (1987). Structure-activity relationships for steroid interaction with the γ-aminobutyric acid-a receptor complex. Journal of Pharmacology and Experimental Therapeutics, 241(1), 346–353.Google Scholar
Hebb, D. O. (1949). Organization of behavior (p. 261). New York: John Wiley and Sons.Google Scholar
Ikonomidou, C., Mosinger, L. L., Shahid Sallett, K., Labruyere, J., & Olney, J. W. (1989). Sensitivity of the developing rat brain to hyperbaric/ischemic damage parallels sensitivity to N-methyl-Daspartate neurotoxicity. Journal of Neuroscience, 9, 2809–2818.CrossRefGoogle Scholar
Insel, T. R. (1991). Long-term neural consequences of stress during development: Is early experience a form of chemical imprinting? In Carroll, B. J. & Barrett, J. E. (Eds.), Psychopathology and the brain (pp. 133–152). New York: Raven Press.Google Scholar
Jacobsen, B., & Kinney, D. K. (1980). Perinatal complications in adopted and non-adopted schizophrenics and their controls: Preliminary results. Acta Psychiatrica Scandinavica, 238, 103–123.Google Scholar
Jeste, D., & Lohr, J. B. (1989). Hippocampal pathologic findings in schizophrenia. Archives of General Psychiatry, 46, 1019–1024.CrossRefGoogle ScholarPubMed
Johnston, M. V. (1988). Biochemistry of neurotransmitters in cortical development. In Peters, A. & Jones, E. G. (Eds.), Cerebral cortex (pp. 211–236). New York: Plenum Press.CrossRefGoogle Scholar
Kalivas, P. W., Duffy, P., & Barrow, J. (1989). Regulation of the mesocorticolimbic dopamine system by glutamic acid receptor subtypes. Journal of Pharmacology and Experimental Therapeutics, 251, 378–387.Google ScholarPubMed
Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., & Uylings, H. B. (1988). Development of the dopaminergic innervation in the prefrontal cortex of rat. Journal of Comparative Neurology, 269, 58–72.CrossRefGoogle ScholarPubMed
Kety, S., Rosenthal, D., Wender, P., & Schulsinger, F. (1968). The type and prevalence of mental illness in the biological and adoptive families of adopted schizophrenics. In Rosenthal, D. & Kety, S. (Eds.), The transmission of schizophrenia (pp. 25–37). Oxford: Pergamon Press.Google Scholar
Kovelman, J. A., & Scheibel, A. B. (1984). A neurohistological correlate of schizophrenia. Biological Psychiatry, 19, 1601–1621.Google ScholarPubMed
Lauder, J. M., & Bloom, F. E. (1974). Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. I. Cell differentiation. Journal of Comparative Neurology, 155, 469–482.CrossRefGoogle ScholarPubMed
Levey, N., & Jane, J. (1975). Laminar thermocoagulation of the visual cortex in the rat. Brain Research, 11, 275–321.Google ScholarPubMed
Lopez, J., Chalmers, D., Vazquez, D., Akil, H., & Watson, S. (1993). Chronic unpredictable stress down-regulates serotonin 1A receptors in the hippocampus. Society of Neuroscience Abstracts, 19(1), 216.Google Scholar
Loy, R. (1980). Development of afferent lamination in Ammon's horn of the rat. Anatomy and Embryology, 159, 257–275.CrossRefGoogle ScholarPubMed
Marin-Padilla, M. (1970). Prenatal and early postnatal ontogenesis of the human motor cortex. A Golgi study II. The basket-pyramidal system. Brain Research, 23, 185–191.CrossRefGoogle ScholarPubMed
McDonald, J. W., & Johnston, M. V. (1990). Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Research Reviews, 15, 41–70.CrossRefGoogle ScholarPubMed
Meaney, M. J., Sapolsky, R. M., & McEwen, B. S. (1985a). The development of the glucocorticoid receptor system in the rat limbic brain. I Ontogeny and autoregulation. Developmental Brain Research, 18, 159–164.CrossRefGoogle Scholar
Meaney, M. J., Sapolsky, R. M., & McEwen, B. S. (1985b). The development of the glucocorticoid receptor system in the rat limbic brain. II. An autoradiographic study. Developmental Brain Research, 18, 165–168.CrossRefGoogle Scholar
Meltzer, H. Y., Matsubara, S., & Lee, J. C. (1989). Classification of typical and a typical antipsychotic drugs on the basis of dopamine D-1, D-2 and serotonin-2 pKi values. Journal of Pharmacology and Experimental Therapeutics, 43, 587–604.Google Scholar
Milner, T. A., Loy, R., & Amaral, D. G. (1983). An anatomical study of the development of the septohippocampal projection in the rat. Developmental Brain Research, 8, 343–371.CrossRefGoogle Scholar
Mita, T., Hanada, S., Nishino, N., Kuno, T., Nakai, H., Yamadori, T., Mizoi, Y., & Tanaka, C. (1986). Decreased serotonin S2 and increased dopamine D2 receptors in chronic schizophrenics. Biological Psychiatry, 21, 1407–1414.CrossRefGoogle ScholarPubMed
Monaghan, D. T., Cotman, C. W. (1985). Distribution of N-methyl-D-aspartate-sensitive L-3H-glutamate-binding sites in rat brain. Journal of Neuroscience, 5, 2905–2919.CrossRefGoogle ScholarPubMed
Morilak, D. A., Garlow, S. J., & Ciaranello, R. D. (1994). Immunocytochemical localization and description of neurons expressing 5-HT-2 receptors in the rat brain. Neuroscience, 54, 701–717.CrossRefGoogle Scholar
Olney, J. W., Sesma, M. A., & Wozniak, D. F. (1993). Glutamatergic, cholinergic and GABAergic systems in posterior cingulate cortex: Interactions and possible mechanisms of limbic system disease. In Vogt, B. A. & Gabriel, M. (Eds.), The neurobiology of cingulate cortex and limbic thalamus (pp. 557–580). Boston: Birkhauser.CrossRefGoogle Scholar
Olpe, H. (1981). The cortical projection of the dorsalraphe nucleus: Some electrophysiological and pharmacological properties. Brain Research, 216, 61–71.CrossRefGoogle Scholar
Palacios, J. M., Niehoff, D. L., & Kuhar, M. J. (1979). Ontogeny of GABA and benzodiazepine receptors: Effects of Triton X-100, bromide and muscimol. Brain Research, 179, 390–395.CrossRefGoogle ScholarPubMed
Parnas, J., Schulsinger, F., Teasdale, W., Schulsinger, H., Feldman, P. M., & Mednick, S. A. (1982). Perinatal complications and clinical outcome. British Journal of Psychiatry, 140, 416–420.CrossRefGoogle ScholarPubMed
Rakic, P. (1981). Developmental events leading to laminar and area organization of the neocortex. In Schmitt, F. O. (Ed.), The organization of the cerebral cortex (pp. 7–28). Cambridge: MIT Press.Google Scholar
Rakic, P., & Nowakowski, R. (1981). The time of origin of neurons in the hippocampal region of the rhesus monkey. Journal of Comparative Neurology, 196, 99–128.CrossRefGoogle ScholarPubMed
Represa, A., Tremblay, E., & Ben-Ari, Y. (1989). Transient increase of NMDA-binding sites in human hippocampus during development. Neuroscience Letters, 99, 61–66.CrossRefGoogle ScholarPubMed
Retaux, S., Besson, M. J., & Penit-Soria, J. (1991a). Opposing effects of dopamine D2 receptor stimulation on the spontaneous and the electrically evoked release of [3H]GABA on rat prefrontal cortex slices. Neuroscience, 42(1), 61–71.CrossRefGoogle ScholarPubMed
Retaux, S., Besson, M. J., & Penit-Soria, J. (1991b). Synergism between Dl and D2 dopamine receptors in the inhibition of the evoked release of [3H]GABA in the rat prefrontal cortex. Neuroscience, 43 (2/3), 323–329.CrossRefGoogle Scholar
Roth, R. H., Tarn, S. Y., Ida, Y., Yang, J. X., & Deutch, A. Y. (1988). Stress and the mesocorticolimbic dopamine systems. Annals of the New York Academy of Sciences, 537, 138–147.CrossRefGoogle ScholarPubMed
Rozenberg, F., Robain, O., Jardin, L., & Ben-Ari, Y. (1989). Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Developmental Brain Research, 50, 177–187.CrossRefGoogle ScholarPubMed
Sapolsky, R. (1986). Glucocorticoid toxicity in the hippocampus: Temporal aspects of synergy with kainic acid. Neuroendocrinology, 43, 386–392.CrossRefGoogle ScholarPubMed
Sapolsky, R. M. (1992). Stress, the aging brain, and the mechanisms of neuron death. Cambridge: MIT Press.Google Scholar
Sawaguchi, T., Matsumura, M., & Kubota, K. (1990). Effects of dopamine antagonists on neuronal activity related to a delayed response task in monkey prefrontal cortex. Journal of Neurophysiology, 63 (6), 1401–1412.CrossRefGoogle ScholarPubMed
Scheff, S., Joff, S., & Anderson, K. (1986). Altered regulation of lesion-induced synaptogenesis by adrenalectomy and corticosterone in young adult rats. Experimental Neurology, 93, 456–470.CrossRefGoogle ScholarPubMed
Schwartz, R., Wess, M., Labarca, R., Skolnick, P., & Paul, S. (1987). Acute stress enhances the activity of the GABA receptor-gated ion channel in brain. Brain Research, 411, 151–155.CrossRefGoogle ScholarPubMed
Selye, H. (1936). A syndrome produced by diverse nocuous agents. Nature (London), 138, 32.CrossRefGoogle Scholar
Seress, L., & Ribak, C. E. (1988). The development of GABAergic neurons in the rat hippocampal formation. An immunocytochemical study. Development Brain Research, 44, 197–202.CrossRefGoogle ScholarPubMed
Sheldon, P. W., & Aghajanian, G. K. (1990). Serotonin (5-HT) induces IPSPs in pyramidal layer cells of rat piriform cortex: Evidence for the involvement of a 5-HT2-activated interneuron. Brain Research, 506, 62–69.CrossRefGoogle ScholarPubMed
Shepherd, G. M. (Ed.). (1990). The synoptic organization of the brain. New York: Oxford University Press.Google Scholar
Sillito, A. M. (1984). Functional considerations of the operation of GABAergic inhibitory processes in the visual cortex. In Jones, E. G. & Peters, A. (Eds.), Cerebral cortex (pp. 91–118). New York: Plenum Press.CrossRefGoogle Scholar
Soriano, E., Cobas, S. A., & Fairen, A. (1986). Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Developmental Brain Research, 30, 88–92.CrossRefGoogle Scholar
Stein-Behrens, B., Elliott, E., Miller, C., Schilling, J., Newcombe, R., & Sapolsky, R. (1992). Glucocorticoids exacerbate kainic acid-induced extracellular accumulation of excitatory amino acids in the rat hippocampus. Journal of Neurochemistry, 58, 1730–1734.CrossRefGoogle ScholarPubMed
Steiner, H. X., McBean, G. J., Kohler, C., Roberts, P. J., & Schwarcz, R. (1984). Ibotenate-induced neuronal degeneration in immature rat brain. Brain Research, 307, 117–124.CrossRefGoogle ScholarPubMed
Swann, J. W., Brady, R. J., & Martin, D. L. (1989). Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience, 25(3), 551–561.CrossRefGoogle Scholar
Takahashi, L. K., & Kalin, N. H. (1991). Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Research, 558, 75–78.CrossRefGoogle ScholarPubMed
Thierry, A. M., Tassin, J. P., Blanc, G., & Glowinski, J. (1976). Selective activation of the mesocortical DA system by stress. Nature (London), 263, 242–244.CrossRefGoogle ScholarPubMed
Traber, J., & Glaser, T. (1987). 5-HT1A receptor-related anxiolytics. Trends in Pharmacology, 8, 432–437.CrossRefGoogle Scholar
Uno, H., Lohmiller, L., Thieme, C., Kemnitz, J., Engle, M., Roecker, E., & Farrell, P. (1990). Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Developmental Brain Research, 53, 157–167.CrossRefGoogle ScholarPubMed
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
Vijayan, V., & Cotman, C. (1987). Hydricortisone administration alters glial reaction to entorhinal lesion in the rat dentate gyrus. Experimental Neurology, 96, 307.CrossRefGoogle ScholarPubMed
Vincent, S. L., Khan, Y., & Benes, F. M. (1993). Cellular distribution of dopamine Dl and D2 receptors in rat medial prefrontal cortex. Journal of Neuro-science, 13, 2551–2561.Google Scholar
Virgin, C. E. Jr., Ha, T. P.-T., Packan, D. R., Tombaugh, G. C., Yang, S. H., Horner, H. C., & Sapolsky, R. M. (1991). Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: Implications for glucocorticoid neurotoxicity. Journal of Neurochemistry, 57(4), 1422–1428.CrossRefGoogle ScholarPubMed
Vogt, B. A. (1991). The role of Layer I in cortical function. In Cerebral cortex. Normal and altered functional states (Vol. 9, pp. 49–80). New York: Plenum Press.CrossRefGoogle Scholar
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., Herman, K. F., & Zec, 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
Whitaker, P. M., Crow, T., & Ferrier, I. N. (1981). Tritiated LSD binding in frontal cortex in schizophrenia. Archives of General Psychiatry, 38, 278–280.CrossRefGoogle ScholarPubMed
Young, A. B., Dauth, G. W., Hollingsworth, Z., Penney, J. B., Kaatz, K., & Gilman, S. (1990). Quisqualate- and NMDA-sensitive [3H] glutamate binding in primate brain. Journal of Neuroscience Research, 27, 512–521.CrossRefGoogle ScholarPubMed