Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration.

Chronic stress produces deficits in cognition accompanied by alterations in neural chemistry and morphology. For example, both stress and chronic administration of corticosterone produce dendritic atrophy in hippocampal neurons (Woolley C, Gould E, McEwen BS. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225-231; Watanabe Y, Gould E, McEwen BS, 1992b. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345). Prefrontal cortex is also a target for glucocorticoids involved in the stress response (Meaney MJ, Aitken DH. 1985. [(3)H]Dexamethasone binding in rat frontal cortex. Brain Res 328:176-180); it shows neurochemical changes in response to stress (e.g., Luine VN, Spencer RL, McEwen BS. 1993. Effect of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res 616:55-70; Crayton JW, Joshi I, Gulati A, Arora RC, Wolf WA. 1996. Effect of corticosterone on serotonin and catecholamine receptors and uptake sites in rat frontal cortex. Brain Res 728:260-262; Takao K, Nagatani T, Kitamura Y, Yamawaki S. 1997. Effects of corticosterone on 5-HT(1A) and 5-HT(2) receptor binding and on the receptor-mediated behavioral responses of rats. Eur J Pharmacol 333:123-128; Sandi C, Loscertales M. 1999. Opposite effects on NCAM expression in the rat frontal cortex induced by acute vs. chronic corticosterone treatments. Brain Res 828:127-134), and mediates many of the behaviors that are altered by chronic corticosterone administration (e.g., Lyons DM, Lopez JM, Yang C, Schatzberg AF. 2000. Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys. J Neurosci 20:7816-7821). To determine if glucocorticoid-induced morphological changes also occur in medial prefrontal cortex, the effects of chronic corticosterone administration on dendritic morphology in this corticolimbic structure were assessed. Adult male rats received s.c. injections of either corticosterone (10 mg in 250 microL sesame oil; n = 8) or vehicle (250 microL; n = 8) daily for 3 weeks. A third group of rats served as intact controls (n = 4). Brains were stained using a Golgi-Cox procedure and pyramidal neurons in layer II-III of medial prefrontal cortex were drawn; dendritic morphology was quantified in three dimensions. Sholl analyses demonstrated a significant redistribution of apical dendrites in corticosterone-treated animals: the amount of dendritic material proximal to the soma was increased relative to intact rats, while distal dendritic material was decreased relative to intact animals. Thus, chronic glucocorticoid administration dramatically reorganized apical arbors in medial prefrontal cortex. This reorganization likely reflects functional changes and may contribute to stress-induced changes in cognition.

[1]  L. Swanson,et al.  A direct projection from Ammon's horn to prefrontal cortex in the rat , 1981, Brain Research.

[2]  H. Mayberg Limbic-cortical dysregulation: a proposed model of depression. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[3]  Y. Watanabe,et al.  Tianeptine attenuates stress-induced morphological changes in the hippocampus. , 1992, European journal of pharmacology.

[4]  J. Mazziotta,et al.  Reduction of prefrontal cortex glucose metabolism common to three types of depression. , 1989, Archives of general psychiatry.

[5]  C. Sandi,et al.  Opposite effects on NCAM expression in the rat frontal cortex induced by acute vs. chronic corticosterone treatments , 1999, Brain Research.

[6]  M. Seligman,et al.  Failure to escape traumatic shock. , 1967, Journal of experimental psychology.

[7]  G. Brown,et al.  Crises and life changes and the onset of schizophrenia. , 1968, Journal of health and social behavior.

[8]  B. Moghaddam,et al.  Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam , 1997, Neuroscience.

[9]  P. Henke Granule cell potentials in the dentate gyrus of the hippocampus: Coping behavior and stress ulcers in rats , 1990, Behavioural Brain Research.

[10]  G. Paxinos The Rat nervous system , 1985 .

[11]  Takeshi Inoue,et al.  Effects of acute and chronic administration of high-dose corticosterone and dexamethasone on regional brain dopamine and serotonin metabolism in rats , 1996, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[12]  B. Mcewen,et al.  Stress‐Dependent Impairments of Spatial Memory. Role of 5‐HT , 1994, Annals of the New York Academy of Sciences.

[13]  T. Harris,et al.  Life events and illness , 1990 .

[14]  H. Groenewegen Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography , 1988, Neuroscience.

[15]  B. McEwen,et al.  Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews , 1996, The Journal of Neuroscience.

[16]  R. Guillery Histology of the Nervous System by Santiago Ramón y Cajal. Translated into English from the French edition by Neely Swanson and Larry W. Swanson, Oxford University Press, 1995. $195.00 (1672 pp) ISBN 0 19 507 4017 , 1996, Trends in Neurosciences.

[17]  R. Rosellini Inescapable shock interferes with the acquisition of an appetitive operant , 1978 .

[18]  A. Scheibel,et al.  Of Pattern and Place in Dendrites12 , 1970 .

[19]  S Levine,et al.  Behavioral stress impairs long-term potentiation in rodent hippocampus. , 1987, Behavioral and neural biology.

[20]  B. McEwen,et al.  Chronic exposure to stress levels of corticosterone alters GABAA receptor subunit mRNA levels in rat hippocampus. , 1995, Brain research. Molecular brain research.

[21]  B. McEwen,et al.  Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function , 1993, Brain Research.

[22]  N. Sousa,et al.  Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement , 2000, Neuroscience.

[23]  M. Joëls,et al.  Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. , 1989, Science.

[24]  A. Stone,et al.  Changes in daily event frequency precede episodes of physical symptoms. , 1987, Journal of human stress.

[25]  S. Yamawaki,et al.  Effects of corticosterone on 5-HT1A and 5-HT2 receptor binding and on the receptor-mediated behavioral responses of rats. , 1997, European journal of pharmacology.

[26]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged and fatal stress in primates , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  A C Roberts,et al.  Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. , 1996, Behavioral neuroscience.

[28]  Paul D. Coleman,et al.  Neuron numbers and dendritic extent in normal aging and Alzheimer's disease , 1987, Neurobiology of Aging.

[29]  R. Hauger,et al.  Differential regulation of brain and pituitary corticotropin-releasing factor receptors by corticosterone. , 1987, Endocrinology.

[30]  D. M. Lyons,et al.  Stress-Level Cortisol Treatment Impairs Inhibitory Control of Behavior in Monkeys , 2000, The Journal of Neuroscience.

[31]  J. Price An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex , 1973, The Journal of comparative neurology.

[32]  Edmund M. Glaser,et al.  Analysis of thick brain sections by obverse—Reverse computer microscopy: Application of a new, high clarity Golgi—Nissl stain , 1981, Journal of Neuroscience Methods.

[33]  B. Moghaddam,et al.  Stress Preferentially Increases Extraneuronal Levels of Excitatory Amino Acids in the Prefrontal Cortex: Comparison to Hippocampus and Basal Ganglia , 1993, Journal of neurochemistry.

[34]  J. Seamans,et al.  Contributions of Voltage-Gated Ca2+ Channels in the Proximal versus Distal Dendrites to Synaptic Integration in Prefrontal Cortical Neurons , 1997, The Journal of Neuroscience.

[35]  B. Moghaddam,et al.  Glutamatergic Control of Dopamine Release During Stress in the Rat Prefrontal Cortex , 1994, Journal of neurochemistry.

[36]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[37]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[38]  E. Kay,et al.  The generality of learned helplessness in the rat , 1977 .

[39]  B. McEwen,et al.  Rat Brain Binds Adrenal Steroid Hormone: Radioautography of Hippocampus with Corticosterone , 1972, Science.

[40]  K. Nuechterlein,et al.  A prospective study of stressful life events and schizophrenic relapse. , 1989, Journal of abnormal psychology.

[41]  S. Cajal,et al.  Histology of the Nervous System , 1911 .

[42]  E. P. Gardner The organization of the cerebral cortex Eds F. O. Schmitt, F. G. Worden, G. Adelman and S. G. Dennis. MIT Press, Cambridge, MA: 1981. 592 pp. $50.00, £31.00 , 1982, Neuroscience.

[43]  Bruce S. McEwen,et al.  Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons , 1990, Brain Research.

[44]  P. Bailey,et al.  Organization of the cerebral cortex. , 1948, The Proceedings of the Institute of Medicine of Chicago.

[45]  Richard F. Thompson,et al.  Manipulation of Pituitary-Adrenal Activity Affects Neural Plasticity in Rodent Hippocampus , 1990 .

[46]  B. McEwen,et al.  Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors , 1995, Neuroscience.

[47]  M. Ferrini,et al.  Chronic Corticosterone Impairs Inhibitory Avoidance in Rats Possible Link With Atrophy of Hippocampal CA3 Neurons , 2000, Pharmacology Biochemistry and Behavior.

[48]  Adolf Pfefferbaum,et al.  Neuroimaging studies of schizophrenia , 1991, Schizophrenia Research.

[49]  J. Csernansky,et al.  Chronic corticosterone treatment impairs spontaneous alternation behavior in rats. , 1994, Behavioral and neural biology.

[50]  T. Kadar,et al.  Cognitive deficits induced in young rats by long-term corticosterone administration. , 1993, Behavioral and neural biology.

[51]  J. Eberwine,et al.  Corticosteroid Regulation of Ion Channel Conductances and mRNA Levels in Individual Hippocampal CA1 Neurons , 1998, The Journal of Neuroscience.

[52]  M. Meaney,et al.  [3H]Dexamethasone binding in rat frontal cortex , 1985, Brain Research.

[53]  Bruce S. McEwen,et al.  Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons , 1992, Brain Research.

[54]  Ramesh Chandra Arora,et al.  Effect of corticosterone on serotonin and catecholamine receptors and uptake sites in rat frontal cortex , 1996, Brain Research.