Dendritic spine pathology in schizophrenia

Neuroscience

Volumn 251, Issue , 2013, Pages 90-107

  Glausier, J R ^a   Lewis, D A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Development; Laminar; Medium spiny neuron; Pruning; Pyramidal cell; Spinogenesis

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HALOPERIDOL; KALIRIN; MESSENGER RNA; NEUROLEPTIC AGENT; OLANZAPINE; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANHEDONIA; BLUNTED AFFECT; BRAIN SIZE; CELL DENSITY; CLINICAL FEATURE; COGNITIVE DEFECT; DELUSION; DENDRITIC SPINE; GOLGI STAIN; HALLUCINATION; HEREDITY; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HUMAN; MOLECULAR MECHANICS; NEOCORTEX; NONHUMAN; PATHOPHYSIOLOGY; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; REVIEW; RISK FACTOR; SCHIZOPHRENIA; SPEECH DISORDER; THOUGHT DISORDER; TREATMENT OUTCOME;

22Q11 DELETION SYNDROME; 22Q11 DS; ANTIPSYCHOTIC DRUGS; APDS; DEVELOPMENT; DISC1; DISRUPTED IN SCHIZOPHRENIA 1; DLPFC; DORSOLATERAL PREFRONTAL CORTEX; GEFS; GUANINE EXCHANGE FACTORS; LAMINAR; MAGNETIC RESONANCE IMAGING; MD; MEDIODORSAL; MEDIUM SPINY NEURON; MEDIUM SPINY NEURONS; MFT; MOSSY FIBER TERMINATIONS; MRI; MSN; PFC; PMI; POSTMORTEM INTERVALS; PREFRONTAL CORTEX; PRUNING; PYRAMIDAL CELL; SP-IR; SPINOGENESIS; SPINOPHILIN-IMMUNOREACTIVE; TDL; TOTAL DENDRITIC LENGTH; VENTRAL TEGMENTAL AREA; VTA;

DENDRITIC SPINES; HUMANS; NEOCORTEX; PYRAMIDAL CELLS; SCHIZOPHRENIA;

EID: 84884288041     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.04.044     Document Type: Review

References (243)

1. Abi-Dargham A., Mawlawi O., Lombardo I., Gill R., Martinez D., Huang Y., Hwang D.R., Keilp J., Kochan L., van Heertum R., Gorman J.M., Laruelle M. Prefrontal dopamine D1 receptors and working memory in schizophrenia. J Neurosci 2002, 22:3708-3719.
2. Abi-Dargham A, Xu X, Thompson JL, Gil R, Kegeles LS, Urban NB, Narendran R, Hwang DR, Laruelle M, Slifstein M (2011) Increased prefrontal cortical D1 receptors in drug naive patients with schizophrenia: a PET study with [11C]NNC112. J Psychopharmacol [epub ahead of print].
3. Ahmed B., Anderson J.C., Douglas R.J., Martin K.A.C., Nelson J.C. Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol 1994, 341:39-49.
4. Akil M., Pierri J.N., Whitehead R.E., Edgar C.L., Mohila C., Sampson A.R., Lewis D.A. Lamina-specific alterations in the dopamine innervation of the prefrontal cortex in schizophrenic subjects. Am J Psychiatry 1999, 156:1580-1589.
5. Aleman A., Kahn R.S., Selten J.P. Sex differences in the risk of schizophrenia: evidence from meta-analysis. Arch Gen Psychiatry 2003, 60:565-571.
6. Allen N.J., Barres B.A. Signaling between glia and neurons: focus on synaptic plasticity. Curr Opin Neurobiol 2005, 15:542-548.
7. American Psychiatric Association DSM-IV. Diagnostic and statistical manual of mental disorders 1994, American Psychiatric Association, Washington, DC. 4th ed.
8. Andersen B.B., Pakkenberg B. Stereological quantitation in cerebella from people with schizophrenia. Br J Psychiatry 2003, 182:354-361.
9. Anderson S.A., Classey J.D., Condé F., Lund J.S., Lewis D.A. Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience 1995, 67:7-22.
10. Arion D., Unger T., Lewis D.A., Mirnics K. Molecular markers distinguishing supragranular and infragranular layers in the human prefrontal cortex. Eur J Neurosci 2007, 25:1843-1854.
11. Arnsten A.F., Paspalas C.D., Gamo N.J., Yang Y., Wang M. Dynamic network connectivity: a new form of neuroplasticity. Trends Cogn Sci 2010, 14:365-375.
12. Arnsten A.F.T., Cai J.S., Goldman-Rakic P.S. The alpha-2 adrenergic agonist guanfacine improves memory in aged monkeys without sedative or hypotensive side effects: evidence for alpha-2 receptor subtypes. J Neurosci 1988, 8:4287-4298.
13. Atkin T.A., MacAskill A.F., Brandon N.J., Kittler J.T. Disrupted in schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons. Mol Psychiatry 2011, 16(122-4):121.
14. Awad A.G., Voruganti L.N. The burden of schizophrenia on caregivers: a review. Pharmacoeconomics 2008, 26:149-162.
15. Baker K., Chaddock C.A., Baldeweg T., Skuse D. Neuroanatomy in adolescents and young adults with 22q11 deletion syndrome: comparison to an IQ-matched group. NeuroImage 2011, 55:491-499.
16. Balu DT, Basu AC, Corradi JP, Cacace AM, Coyle JT (2011) The NMDA receptor co-agonists, d-serine and glycine, regulate neuronal dendritic architecture in the somatosensory cortex. Neurobiol Dis [epub ahead of print].
17. Baracskay K.L., Haroutunian V., Meador-Woodruff J.H. Dopamine receptor signaling molecules are altered in elderly schizophrenic cortex. Synapse 2006, 60:271-279.
18. Bauer D., Gupta D., Harotunian V., Meador-Woodruff J.H., McCullumsmith R.E. Abnormal expression of glutamate transporter and transporter interacting molecules in prefrontal cortex in elderly patients with schizophrenia. Schizophr Res 2008, 104:108-120.
19. Bennett M.R. Schizophrenia: susceptibility genes, dendritic-spine pathology and gray matter loss. Prog Neurobiol 2011, 95:275-300.
20. Bernstein H.G., Steiner J., Bogerts B. Glial cells in schizophrenia: pathophysiological significance and possible consequences for therapy. Expert Rev Neurother 2009, 9:1059-1071.
21. Bogerts B., Meertz E., Schönfeldt-Bausch R. Basal ganglia and limbic system pathology in schizophrenia. A morphometric study of brain volume and shrinkage. Arch Gen Psychiatry 1985, 42:784-791.
22. Bolam J.P., Hanley J.J., Booth P.A., Bevan M.D. Synaptic organisation of the basal ganglia. J Anat 2000, 196(Pt. 4):527-542.
23. Bongmba O.Y., Martinez L.A., Elhardt M.E., Butler K., Tejada-Simon M.V. Modulation of dendritic spines and synaptic function by Rac1: a possible link to Fragile X syndrome pathology. Brain Res 2011, 1399:79-95.
24. Borgwardt S.J., Picchioni M.M., Ettinger U., Toulopoulou T., Murray R., McGuire P.K. Regional gray matter volume in monozygotic twins concordant and discordant for schizophrenia. Biol Psychiatry 2010, 67:956-964.
25. Borgwardt S.J., Riecher-Rossler A., Dazzan P., Chitnis X., Aston J., Drewe M., Gschwandtner U., Haller S., Pfluger M., Rechsteiner E., D'Souza M., Stieglitz R.D., Radu E.W., McGuire P.K. Regional gray matter volume abnormalities in the at risk mental state. Biol Psychiatry 2007, 61:1148-1156.
26. Bourgeois J.-P., Goldman-Rakic P.S., Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 1994, 4:78-96.
27. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr Opin Neurobiol 2007, 17:381-386.
28. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 2008, 31:47-67.
29. Brandt G.N., Bonelli R.M. Structural neuroimaging of the basal ganglia in schizophrenic patients: a review. Wien Med Wochenschr 2008, 158:84-90.
30. Brennaman L.H., Kochlamazashvili G., Stoenica L., Nonneman R.J., Moy S.S., Schachner M., Dityatev A., Maness P.F. Transgenic mice overexpressing the extracellular domain of NCAM are impaired in working memory and cortical plasticity. Neurobiol Dis 2011, 43:372-378.
31. Broadbelt K., Byne W., Jones L.B. Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res 2002, 58:75-81.
32. Buell S.J. Golgi-Cox and rapid golgi methods as applied to autopsied human brain tissue: widely disparate results. J Neuropathol Exp Neurol 1982, 41:500-507.
33. Byne W., Buchsbaum M.S., Mattiace L.A., Hazlett E.A., Kemether E., Elhakem S.L., Purohit D.P., Haroutunian V., Jones L. Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. Am J Psychiatry 2002, 159:59-65.
34. Cahill M.E., Jones K.A., Rafalovich I., Xie Z., Barros C.S., Muller U., Penzes P. Control of interneuron dendritic growth through NRG1/erbB4-mediated kalirin-7 disinhibition. Mol Psychiatry 2012, 17:99-107.
35. Cahill M.E., Xie Z., Day M., Photowala H., Barbolina M.V., Miller C.A., Weiss C., Radulovic J., Sweatt J.D., Disterhoft J.F., Surmeier D.J., Penzes P. Kalirin regulates cortical spine morphogenesis and disease-related behavioral phenotypes. Proc Natl Acad Sci USA 2009, 106:13058-13063.
36. Calabrese B., Wilson M.S., Halpain S. Development and regulation of dendritic spine synapses. Physiology (Bethesda) 2006, 21:38-47.
37. Cannon T.D., Thompson P.M., van Erp T.G.M., Toga A.W., Poutanen V.-P., Huttunen M., Lonnqvist J., Standertskjold-Nordenstam C.-G., Narr K.L., Khaledy M., Zoumalan C.I., Dail R., Kaprio J. Cortex mapping reveals regionally specific patterns of genetic and disease-specific gray-matter deficits in twins discordant for schizophrenia. Proc Natl Acad Sci USA 2002, 99:3228-3233.
38. Cardno A.G., Marshall E.J., Coid B., MacDonald A.M., Ribchester T.R., Davies N.J., Venturi P., Jones L.A., Lewis S.W., Sham P.C., Gottesman I.I., Farmer A.E., McGuffin P., Reveley A.M., Murray R.M. Heritability estimates for psychotic disorders: the Maudsley twin psychosis series. Arch Gen Psychiatry 1999, 56:162-168.
39. Casadio P., Fernandes C., Murray R.M., Di Forti M. Cannabis use in young people: the risk for schizophrenia. Neurosci Biobehav Rev 2011, 35:1779-1787.
40. Casey B.J., Jones R.M., Levita L., Libby V., Pattwell S.S., Ruberry E.J., Soliman F., Somerville L.H. The storm and stress of adolescence: insights from human imaging and mouse genetics. Dev Psychobiol 2010, 52:225-235.
41. Cerri C., Fabbri A., Vannini E., Spolidoro M., Costa M., Maffei L., Fiorentini C., Caleo M. Activation of Rho GTPases triggers structural remodeling and functional plasticity in the adult rat visual cortex. J Neurosci 2011, 31:15163-15172.
42. Cheng A., Hou Y., Mattson M.P. Mitochondria and neuroplasticity. ASN Neuro 2010, 2.
43. Cheng H.W., Rafols J.A., Goshgarian H.G., Anavi Y., Tong J., McNeill T.H. Differential spine loss and regrowth of striatal neurons following multiple forms of deafferentation: a Golgi study. Exp Neurol 1997, 147:287-298.
44. Cho R.Y., Konecky R.O., Carter C.S. Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci USA 2006, 103:19878-19883.
45. Chu-Shore C.J., Kramer M.A., Bianchi M.T., Caviness V.S., Cash S.S. Network analysis: applications for the developing brain. J Child Neurol 2011, 26:488-500.
46. Chubb J.E., Bradshaw N.J., Soares D.C., Porteous D.J., Millar J.K. The DISC locus in psychiatric illness. Mol Psychiatry 2008, 13:36-64.
47. Clay H.B., Sillivan S., Konradi C. Mitochondrial dysfunction and pathology in bipolar disorder and schizophrenia. Int J Dev Neurosci 2011, 29:311-324.
48. Corradini I., Verderio C., Sala M., Wilson M.C., Matteoli M. SNAP-25 in neuropsychiatric disorders. Ann NY Acad Sci 2009, 1152:93-99.
49. Cullen T.J., Walker M.A., Parkinson N., Craven R., Crow T.J., Esiri M.M., Harrison P.J. A postmortem study of the mediodorsal nucleus of the thalamus in schizophrenia. Schizophr Res 2003, 60:157-166.
50. DeFelipe J., Farinas I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 1992, 39:563-607.
51. Deo A.J., Cahill M.E., Li S., Goldszer I., Henteleff R., VanLeeuwen J.E., Rafalovich I., Gao R., Stachowski E.K., Sampson A.R., Lewis D.A., Penzes P., Sweet R.A. Increased expression of Kalirin-9 in the auditory cortex of schizophrenia subjects: its role in dendritic pathology. Neurobiol Dis 2012, 45(2):796-803.
52. DeVito L.M., Balu D.T., Kanter B.R., Lykken C., Basu A.C., Coyle J.T., Eichenbaum H. Serine racemase deletion disrupts memory for order and alters cortical dendritic morphology. Genes Brain Behav 2011, 10:210-222.
53. Dorph-Petersen K.A., Lewis D.A. Stereological approaches to identifying neuropathology in psychosis. Biol Psychiatry 2011, 69:113-126.
54. Dorph-Petersen K.-A., Delevich K.M., Marcsisin M.J., Zhang W., Sampson A.R., Gundersen H.J.G., Lewis D.A., Sweet R.A. Pyramidal neuron number in layer 3 of primary auditory cortex of subjects with schizophrenia. Brain Res 2009, 1285:42-57.
55. Dorph-Petersen K.-A., Pierri J.N., Sun Z., Sampson A.R., Lewis D.A. Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J Comp Neurol 2004, 472:449-462.
56. Drew L.J., Crabtree G.W., Markx S., Stark K.L., Chaverneff F., Xu B., Mukai J., Fenelon K., Hsu P.K., Gogos J.A., Karayiorgou M. The 22q11.2 microdeletion: fifteen years of insights into the genetic and neural complexity of psychiatric disorders. Int J Dev Neurosci 2011, 29:259-281.
57. Dumitriu D., Hao J., Hara Y., Kaufmann J., Janssen W.G., Lou W., Rapp P.R., Morrison J.H. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 2010, 30:7507-7515.
58. Eliez S., Schmitt J.E., White C.D., Reiss A.L. Children and adolescents with velocardiofacial syndrome: a volumetric MRI study. Am J Psychiatry 2000, 157:409-415.
59. Elvevag B., Goldberg T.E. Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 2000, 14:1-21.
60. Fearon P., Kirkbride J.B., Morgan C., Dazzan P., Morgan K., Lloyd T., Hutchinson G., Tarrant J., Fung W.L., Holloway J., Mallett R., Harrison G., Leff J., Jones P.B., Murray R.M. Incidence of schizophrenia and other psychoses in ethnic minority groups: results from the MRC AESOP Study. Psychol Med 2006, 36:1541-1550.
61. Feinberg I. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence?. J Psychiatry Res 1982, 17:319-334.
62. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res Brain Res Rev 2002, 39:29-54.
63. Fornito A., Yung A.R., Wood S.J., Phillips L.J., Nelson B., Cotton S., Velakoulis D., McGorry P.D., Pantelis C., Yucel M. Anatomic abnormalities of the anterior cingulate cortex before psychosis onset: an MRI study of ultra-high-risk individuals. Biol Psychiatry 2008, 64:758-765.
64. Franowicz J.S., Arnsten A.F. The alpha-2a noradrenergic agonist, guanfacine, improves delayed response performance in young adult rhesus monkeys. Psychopharmacology (Berl) 1998, 136:8-14.
65. Friedman J.I., Adler D.N., Temporini H.D., Kemether E., Harvey P.D., White L., Parrella M., Davis K.L. Guanfacine treatment of cognitive impairment in schizophrenia. Neuropsychopharmacology 2001, 25:402-409.
66. Fung S.J., Sivagnanasundaram S., Weickert C.S. Lack of change in markers of presynaptic terminal abundance alongside subtle reductions in markers of presynaptic terminal plasticity in prefrontal cortex of schizophrenia patients. Biol Psychiatry 2011, 69:71-79.
67. Garcia-Lopez P., Garcia-Marin V., Freire M. Dendritic spines and development: towards a unifying model of spinogenesis - a present day review of Cajal's histological slides and drawings. Neural Plast 2010, 2010:769207.
68. Garey L.J., Ong W.Y., Patel T.S., Kanani M., Davis A., Mortimer A.M., Barnes T.R.E., Hirsch S.R. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry 1998, 65:446-453.
69. Gigante A.D., Andreazza A.C., Lafer B., Yatham L.N., Beasley C.L., Young L.T. Decreased mRNA expression of uncoupling protein 2, a mitochondrial proton transporter, in post-mortem prefrontal cortex from patients with bipolar disorder and schizophrenia. Neurosci Lett 2011, 505:47-51.
70. Gilbert C.D., Kelly J.P. The projections of cells in different layers of the cat's visual cortex. J Comp Neurol 1975, 63:81-106.
71. Gilmore J.H., Kang C., Evans D.D., Wolfe H.M., Smith J.K., Lieberman J.A., Lin W., Hamer R.M., Styner M., Gerig G. Prenatal and neonatal brain structure and white matter maturation in children at high risk for schizophrenia. Am J Psychiatry 2010, 167:1083-1091.
72. Glahn D.C., Laird A.R., Ellison-Wright I., Thelen S.M., Robinson J.L., Lancaster J.L., Bullmore E., Fox P.T. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry 2008, 64:774-781.
73. Glantz L.A., Lewis D.A. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia: regional and diagnostic specificity. Arch Gen Psychiatry 1997, 54:943-952.
74. Glantz L.A., Lewis D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000, 57:65-73.
75. Goldman-Rakic P.S. Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 1994, 6:348-357.
76. Goldman-Rakic P.S., Leranth C., Williams S.M., Mons N., Geffard M. Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc Natl Acad Sci USA 1989, 86:9015-9019.
77. Goldman-Rakic P.S., Muly E.C., Williams G.V. D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 2000, 31:295-301.
78. Gottesman I.I. Schizophrenia genesis: the origins of madness 1991, W.H. Freeman, New York.
79. Gray E.G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. J Anat 1959, 93:420-433.
80. Green M.F. Cognitive impairment and functional outcome in schizophrenia and bipolar disorder. J Clin Psychiatry 2006, 67(Suppl. 9):3-8.
81. Grossman L.S., Harrow M., Rosen C., Faull R., Strauss G.P. Sex differences in schizophrenia and other psychotic disorders: a 20-year longitudinal study of psychosis and recovery. Compr Psychiatry 2008, 49:523-529.
82. Grutzendler J., Kasthuri N., Gan W.-B. Long-term dendritic spine stability in the adult cortex. Nature 2002, 420:812-816.
83. Hains A.B., Vu M.A., Maciejewski P.K., van Dyck C.H., Gottron M., Arnsten A.F. Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress. Proc Natl Acad Sci USA 2009, 106:17957-17962.
84. Hamori J. The inductive role of presynaptic axons in the development of postsynaptic spines. Brain Res 1973, 62:337-344.
85. Hao J., Rapp P.R., Janssen W.G., Lou W., Lasley B.L., Hof P.R., Morrison J.H. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci USA 2007, 104:11465-11470.
86. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R., Morrison J.H. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 2006, 26:2571-2578.
87. Harris K.M., Kater S.B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 1994, 17:341-371.
88. Harrison P.J. The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl) 2004, 174:151-162.
89. Harvey P.D. Cognitive outcomes in the CATIE schizophrenia trial: why do they seem different from previous results?. Psychiatry (Edgmont) 2007, 4:20-23.
90. Hayashi-Takagi A., Takaki M., Graziane N., Seshadri S., Murdoch H., Dunlop A.J., Makino Y., Seshadri A.J., Ishizuka K., Srivastava D.P., Xie Z., Baraban J.M., Houslay M.D., Tomoda T., Brandon N.J., Kamiya A., Yan Z., Penzes P., Sawa A. Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat Neurosci 2010, 13:327-332.
91. Hayes T.L., Lewis D.A. Magnopyramidal neurons in the anterior motor speech region: dendritic features and interhemispheric comparisons. Arch Neurol 1996, 53:1277-1283.
92. Hill J.J., Hashimoto T., Lewis D.A. Molecular mechanisms contributing to dendritic spine alterations in the prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 2006, 11:557-566.
93. Hoffman R.E., Dobscha S.K. Cortical pruning and the development of schizophrenia: a computer model. Schizophr Bull 1989, 15:477-490.
94. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
95. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry 2005, 162:2233-2245.
96. Horga G., Bernacer J., Dusi N., Entis J., Chu K., Hazlett E.A., Mehmet H.M., Kemether E., Byne W., Buchsbaum M.S. Correlations between ventricular enlargement and gray and white matter volumes of cortex, thalamus, striatum, and internal capsule in schizophrenia. Eur Arch Psychiatry Clin Neurosci 2011, 261:467-476.
97. Horner C.H., Arbuthnott E. Methods of estimation of spine density - are spines evenly distributed throughout the dendritic field?. J Anat 1991, 177:179-184.
98. Hu J., Vidovic M., Chen M.M., Lu Q.Y., Song Z.M. Activation of alpha 2A adrenoceptors alters dendritic spine development and the expression of spinophilin in cultured cortical neurones. Brain Res 2008, 1199:37-45.
99. Hulshoff Pol H.E., Brans R.G., van Haren N.E., Schnack H.G., Langen M., Baare W.F., van Oel C.J., Kahn R.S. Gray and white matter volume abnormalities in monozygotic and same-gender dizygotic twins discordant for schizophrenia. Biol Psychiatry 2004, 55:126-130.
100. Huttenlocher P.R. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 1979, 163:195-205.
101. Huttenlocher P.R., Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 1997, 387:167-178.
102. Ide M., Lewis D.A. Altered cortical CDC42 signaling pathways in schizophrenia: implications for dendritic spine deficits. Biol Psychiatry 2010, 68:25-32.
103. Ikeda M., Aleksic B., Kinoshita Y., Okochi T., Kawashima K., Kushima I., Ito Y., Nakamura Y., Kishi T., Okumura T., Fukuo Y., Williams H.J., Hamshere M.L., Ivanov D., Inada T., Suzuki M., Hashimoto R., Ujike H., Takeda M., Craddock N., Kaibuchi K., Owen M.J., Ozaki N., O'Donovan M.C., Iwata N. Genome-wide association study of schizophrenia in a Japanese population. Biol Psychiatry 2011, 69:472-478.
104. Insel T.R., Scolnick E.M. Cure therapeutics and strategic prevention: raising the bar for mental health research. Mol Psychiatry 2006, 11:11-17.
105. Irie F., Yamaguchi Y. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 2002, 5:1117-1118.
106. Ishihara N., Nomura M., Jofuku A., Kato H., Suzuki S.O., Masuda K., Otera H., Nakanishi Y., Nonaka I., Goto Y., Taguchi N., Morinaga H., Maeda M., Takayanagi R., Yokota S., Mihara K. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 2009, 11:958-966.
107. Jacobs B., Creswell J., Britt J.P., Ford K.L., Bogen J.E., Zaidel E. Quantitative analysis of cortical pyramidal neurons after corpus callosotomy. Ann Neurol 2003, 54:126-130.
108. Jacobs B., Driscoll L., Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 1997, 386:661-680.
109. Jones E.G. Laminar distribution of cortical efferent cells. Cerebral cortex 1984, Vol. 1:521-553. Plenum Press, New York.
110. Kakeda S., Korogi Y. The efficacy of a voxel-based morphometry on the analysis of imaging in schizophrenia, temporal lobe epilepsy, and Alzheimer's disease/mild cognitive impairment: a review. Neuroradiology 2010, 52:711-721.
111. Kalus P., Müller T.J., Zuschratter W., Senitz D. The dendritic architecture of prefrontal pyramidal neurons in schizophrenic patients. NeuroReport 2000, 11:3621-3625.
112. Kane J.M. Schizophrenia. N Engl J Med 1996, 334:34-41.
113. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 2010, 33:121-129.
114. Kasai H., Matsuzaki M., Noguchi J., Yasumatsu N., Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci 2003, 26:360-368.
115. Kasai K., Shenton M.E., Salisbury D.F., Hirayasu Y., Onitsuka T., Spencer M.H., Yurgelun-Todd D.A., Kikinis R., Jolesz F.A., McCarley R.W. Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 2003, 60:766-775.
116. Kates W.R., Antshel K.M., Faraone S.V., Fremont W.P., Higgins A.M., Shprintzen R.J., Botti J.A., Kelchner L., McCarthy C. Neuroanatomic predictors to prodromal psychosis in velocardiofacial syndrome (22q11.2 deletion syndrome): a longitudinal study. Biol Psychiatry 2011, 69:945-952.
117. Kates W.R., Burnette C.P., Jabs E.W., Rutberg J., Murphy A.M., Grados M., Geraghty M., Kaufmann W.E., Pearlson G.D. Regional cortical white matter reductions in velocardiofacial syndrome: a volumetric MRI analysis. Biol Psychiatry 2001, 49:677-684.
118. Keefe R.S., Bilder R.M., Davis S.M., Harvey P.D., Palmer B.W., Gold J.M., Meltzer H.Y., Green M.F., Capuano G., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., Davis C.E., Hsiao J.K., Lieberman J.A. Neurocognitive effects of antipsychotic medications in patients with chronic schizophrenia in the CATIE Trial. Arch Gen Psychiatry 2007, 64:633-647.
119. Kelley J.J., Gao X.M., Tamminga C.A., Roberts R.C. The effect of chronic haloperidol treatment on dendritic spines in the rat striatum. Exp Neurol 1997, 146:471-478.
120. Keshavan M.S., Diwadkar V.A., Montrose D.M., Stanley J.A., Pettegrew J.W. Premorbid characterization in schizophrenia: the Pittsburgh High Risk Study. World Psychiatry 2004, 3:163-168.
121. Khaitovich P., Lockstone H.E., Wayland M.T., Tsang T.M., Jayatilaka S.D., Guo A.J., Zhou J., Somel M., Harris L.W., Holmes E., Paabo S., Bahn S. Metabolic changes in schizophrenia and human brain evolution. Genome Biol 2008, 9:R124.
122. Kim Y., Zerwas S., Trace S.E., Sullivan P.F. Schizophrenia genetics: where next?. Schizophr Bull 2011, 37:456-463.
123. Kolluri N., Sun Z., Sampson A.R., Lewis D.A. Lamina-specific reductions in dendritic spine density in the prefrontal cortex of subjects with schizophrenia. Am J Psychiatry 2005, 162:1200-1202.
124. Kolomeets N.S., Orlovskaya D.D., Rachmanova V.I., Uranova N.A. Ultrastructural alterations in hippocampal mossy fiber synapses in schizophrenia: a postmortem morphometric study. Synapse 2005, 57:47-55.
125. Kolomeets N.S., Orlovskaya D.D., Uranova N.A. Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse 2007, 61:615-621.
126. Kreczmanski P., Heinsen H., Mantua V., Woltersdorf F., Masson T., Ulfig N., Schmidt-Kastner R., Korr H., Steinbusch H.W.M., Hof P.R., Schmitz C. Volume, neuron density and total neuron number in five subcortical regions in schizophrenia. Brain 2007, 130:678-692.
127. Kreis P., Thevenot E., Rousseau V., Boda B., Muller D., Barnier J.V. The p21-activated kinase 3 implicated in mental retardation regulates spine morphogenesis through a Cdc42-dependent pathway. J Biol Chem 2007, 282:21497-21506.
128. Kritzer M.F., Goldman-Rakic P.S. Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey. J Comp Neurol 1995, 359:131-143.
129. Kulkarni J., Gurvich C., Lee S.J., Gilbert H., Gavrilidis E., de Castella A., Berk M., Dodd S., Fitzgerald P.B., Davis S.R. Piloting the effective therapeutic dose of adjunctive selective estrogen receptor modulator treatment in postmenopausal women with schizophrenia. Psychoneuroendocrinology 2010, 35:1142-1147.
130. Kung L., Force M., Chute D.J., Roberts R.C. Immunocytochemical localization of tyrosine hydroxylase in the human striatum: a postmortem ultrastructural study. J Comp Neurol 1998, 390:52-62.
131. Kushima I, Nakamura Y, Aleksic B, Ikeda M, Ito Y, Shiino T, Okochi T, Fukuo Y, Ujike H, Suzuki M, Inada T, Hashimoto R, Takeda M, Kaibuchi K, Iwata N, Ozaki N (2010) Resequencing and association analysis of the KALRN and EPHB1 genes and their contribution to schizophrenia susceptibility. Schizophr Bull [epub ahead of print].
132. Lawrie S.M., Abukmeil S.S. Brain abnormality in schizophrenia: a systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 1998, 172:110-120.
133. Lesh T.A., Niendam T.A., Minzenberg M.J., Carter C.S. Cognitive control deficits in schizophrenia: mechanisms and meaning. Neuropsychopharmacology 2011, 36:316-338.
134. Leuner B., Gould E. Structural plasticity and hippocampal function. Annu Rev Psychol 2010, 61:111-113.
135. Levitt J.J., Bobrow L., Lucia D., Srinivasan P. A selective review of volumetric and morphometric imaging in schizophrenia. Curr Top Behav Neurosci 2010, 4:243-281.
136. Lewis D.A., Curley A.A., Glausier J.R., Volk D.W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 2012, 35:57-67.
137. Lewis D.A., Gonzalez-Burgos G. Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacol 2008, 33(1):141-165.
138. Lewis D.A., Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 2002, 25:409-432.
139. Lewis D.A., Lieberman J.A. Catching up on schizophrenia: natural history and neurobiology. Neuron 2000, 28:325-334.
140. Li Z., Okamoto K., Hayashi Y., Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004, 119:873-887.
141. Lieberman J.A., Stroup T.S. The NIMH-CATIE schizophrenia study: what did we learn?. Am J Psychiatry 2011, 168:770-775.
142. Lin Y.C., Koleske A.J. Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 2010, 33:349-378.
143. Liston C., Gan W.B. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci USA 2011, 108:16074-16079.
144. Liston C., Miller M.M., Goldwater D.S., Radley J.J., Rocher A.B., Hof P.R., Morrison J.H., McEwen B.S. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006, 26:7870-7874.
145. Lund J.S., Lund R.D., Hendrickson A.E., Bunt A.H., Fuchs A.F. The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 1975, 164:287-304.
146. Marcelis M., Navarro-Mateau F., Murray R., Selten J.-P., van Os J. Urbanization and psychosis: a study of 1942-1978 birth cohorts in The Netherlands. Psychol Med 1998, 28:871-879.
147. Martins-de-Souza D., Harris L.W., Guest P.C., Bahn S. The role of energy metabolism dysfunction and oxidative stress in schizophrenia revealed by proteomics. Antioxid Redox Signal 2011, 15:2067-2079.
148. Matthews D.A., Cotman C., Lynch G. An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts. Brain Res 1976, 115:23-41.
149. Mattson M.P., Gleichmann M., Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766.
150. McGrath J., Saha S., Welham J., El Saadi O., MacCauley C., Chant D. A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med 2004, 2:13.
151. McIntosh A.M., Owens D.C., Moorhead W.J., Whalley H.C., Stanfield A.C., Hall J., Johnstone E.C., Lawrie S.M. Longitudinal volume reductions in people at high genetic risk of schizophrenia as they develop psychosis. Biol Psychiatry 2011, 69:953-958.
152. McKinney R.A., Capogna M., Durr R., Gahwiler B.H., Thompson S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 1999, 2:44-49.
153. Mechelli A., Riecher-Rossler A., Meisenzahl E.M., Tognin S., Wood S.J., Borgwardt S.J., Koutsouleris N., Yung A.R., Stone J.M., Phillips L.J., McGorry P.D., Valli I., Velakoulis D., Woolley J., Pantelis C., McGuire P. Neuroanatomical abnormalities that predate the onset of psychosis: a multicenter study. Arch Gen Psychiatry 2011, 68:489-495.
154. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008, 9:437-452.
155. Melchitzky D.S., González-Burgos G., Barrionuevo G., Lewis D.A. Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex. J Comp Neurol 2001, 430:209-221.
156. Melchitzky D.S., Sesack S.R., Lewis D.A. Parvalbumin-immunoreactive axon terminals in macaque monkey and human prefrontal cortex: laminar, regional and target specificity of type I and type II synapses. J Comp Neurol 1999, 408:11-22.
157. Morgan C., Charalambides M., Hutchinson G., Murray R.M. Migration, ethnicity, and psychosis: toward a sociodevelopmental model. Schizophr Bull 2010, 36:655-664.
158. Mortensen P.B., Pedersen C.B., Westegaard T., Wohlfahrt J., Ewald H., Mors O., Andersen P.K., Melbye M. Effects of family history and place and season of birth on the risk of schizophrenia. N Engl J Med 1999, 340:603-608.
159. Moser M.-B., Trommald M., Andersen P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci USA 1994, 91:12673-12675.
160. Mukai J., Dhilla A., Drew L.J., Stark K.L., Cao L., MacDermott A.B., Karayiorgou M., Gogos J.A. Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion. Nat Neurosci 2008, 11:1302-1310.
161. Nakayama A.Y., Harms M.B., Luo L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J Neurosci 2000, 20:5329-5338.
162. Negishi M., Katoh H. Rho family GTPases and dendrite plasticity. Neuroscientist 2005, 11:187-191.
163. Negyessy L., Goldman-Rakic P.S. Morphometric characterization of synapses in the primate prefrontal cortex formed by afferents from the mediodorsal thalamic nucleus. Exp Brain Res 2005, 164:148-154.
164. O'Neill J., Fitten L.J., Siembieda D.W., Ortiz F., Halgren E. Effects of guanfacine on three forms of distraction in the aging macaque. Life Sci 2000, 67:877-885.
165. Olabi B., Ellison-Wright I., McIntosh A.M., Wood S.J., Bullmore E., Lawrie S.M. Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol Psychiatry 2011, 70:88-96.
166. Pakkenberg B. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 1990, 47:1023-1028.
167. Pantelis C., Velakoulis D., McGorry P.D., Wood S.J., Suckling J., Phillips L.J., Yung A.R., Bullmore E.T., Brewer W., Soulsby B., Desmond P., McGuire P.K. Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 2003, 361:281-288.
168. Pasternak J.F., Woolsey T.A. On the selectivity of the Golgi-Cox method. J Comp Neurol 1975, 160:307-312.
169. Pedersen C.B., Mortensen P.B. Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. Arch Gen Psychiatry 2001, 58:1039-1046.
170. Penzes P., Cahill M.E., Jones K.A., VanLeeuwen J.E., Woolfrey K.M. Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 2011, 14:285-293.
171. Penzes P., Johnson R.C., Sattler R., Zhang X., Huganir R.L., Kambampati V., Mains R.E., Eipper B.A. The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 2001, 29:229-242.
172. Petanjek Z., Judas M., Simic G., Rasin M.R., Uylings H.B., Rakic P., Kostovic I. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA 2011, 108:13281-13286.
173. Peters A. Examining neocortical circuits: some background and facts. J Neurocytol 2002, 31:183-193.
174. Pierri J.N., Volk C.L.E., Auh S., Sampson A., Lewis D.A. Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry 2001, 58:466-473.
175. Piskulic D., Olver J.S., Norman T.R., Maruff P. Behavioural studies of spatial working memory dysfunction in schizophrenia: a quantitative literature review. Psychiatry Res 2007, 150:111-121.
176. Popken G.J., Bunney W.E., Potkin S.G., Jones E.G. Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. Proc Natl Acad Sci USA 2000, 97:9276-9280.
177. Rajkowska G., Selemon L.D., Goldman-Rakic P.S. Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 1998, 55:215-224.
178. Rama P., Linnankoski I., Tanila H., Pertovaara A., Carlson S. Medetomidine, atipamezole, and guanfacine in delayed response performance of aged monkeys. Pharmacol Biochem Behav 1996, 55:415-422.
179. Rapoport J.L., Giedd J.N., Blumenthal J., Hamburger S., Jeffries N., Fernandez T., Nicolson R., Bedwell J., Lenane M., Zijdenbos A., Paus T., Evans A. Progressive cortical change during adolescence in childhood-onset schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 1999, 56:649-654.
180. Rapp P.R., Morrison J.H., Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 2003, 23:5708-5714.
181. Regenold W.T., Phatak P., Marano C.M., Sassan A., Conley R.R., Kling M.A. Elevated cerebrospinal fluid lactate concentrations in patients with bipolar disorder and schizophrenia: implications for the mitochondrial dysfunction hypothesis. Biol Psychiatry 2009, 65:489-494.
182. Regenold W.T., Pratt M., Nekkalapu S., Shapiro P.S., Kristian T., Fiskum G. Mitochondrial detachment of hexokinase 1 in mood and psychotic disorders: implications for brain energy metabolism and neurotrophic signaling. J Psychiatr Res 2012, 46:95-104.
183. Reichenberg A., Caspi A., Harrington H., Houts R., Keefe R.S., Murray R.M., Poulton R., Moffitt T.E. Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: a 30-year study. Am J Psychiatry 2010, 167:160-169.
184. Ren W.W., Liu Y., Li B.M. Stimulation of alpha(2A)-adrenoceptors promotes the maturation of dendritic spines in cultured neurons of the medial prefrontal cortex. Mol Cell Neurosci 2011, 49:205-216.
185. Riecher-Rossler A., Kulkarni J. Estrogens and gonadal function in schizophrenia and related psychoses. Curr Top Behav Neurosci 2011, 8:155-171.
186. Riecher-Rossler A., Loffler W., Munk-Jorgensen P. What do we really know about late-onset schizophrenia?. Eur Arch Psychiatry Clin Neurosci 1997, 247:195-208.
187. Roberts R.C., Conley R., Kung L., Peretti F.J., Chute D.J. Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study. NeuroReport 1996, 7:1214-1218.
188. Roberts R.C., Gaither L.A., Gao X.M., Kashyap S.M., Tamminga C.A. Ultrastructural correlates of haloperidol-induced oral dyskinesias in rat striatum. Synapse 1995, 20:234-243.
189. Roberts R.C., Roche J.K., Conley R.R. Synaptic differences in the patch matrix compartments of subjects with schizophrenia: a postmortem ultrastructural study of the striatum. Neurobiol Dis 2005, 20:324-335.
190. Roberts R.C., Roche J.K., Conley R.R. Synaptic differences in the postmortem striatum of subjects with schizophrenia: a stereological ultrastructural analysis. Synapse 2005, 56:185-197.
191. Roberts R.C., Roche J.K., Conley R.R. Differential synaptic changes in the striatum of subjects with undifferentiated versus paranoid schizophrenia. Synapse 2008, 62:616-627.
192. Rosenfeld M., Brenner-Lavie H., Ari S.G., Kavushansky A., Ben Shachar D. Perturbation in mitochondrial network dynamics and in complex I dependent cellular respiration in schizophrenia. Biol Psychiatry 2011, 69:980-988.
193. Rosoklija G., Toomayan G., Ellis S.P., Keilp J., Mann J.J., Latov N., Hays A.P., Dwork A.J. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 2000, 57:349-356.
194. Rubino T., Realini N., Braida D., Guidi S., Capurro V., Vigano D., Guidali C., Pinter M., Sala M., Bartesaghi R., Parolaro D. Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus 2009, 19:763-772.
195. Sa S.I., Pereira P.A., Paula-Barbosa M.M., Madeira M.D. Role of neural afferents as mediators of estrogen effects on the hypothalamic ventromedial nucleus. Brain Res 2010, 1366:60-70.
196. Saha S., Chant D., Welham J., McGrath J. A systematic review of the prevalence of schizophrenia. PLoS Med 2005, 2:e141.
197. Salisbury D.F., Kuroki N., Kasai K., Shenton M.E., McCarley R.W. Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. Arch Gen Psychiatry 2007, 64:521-529.
198. Scott E.K., Reuter J.E., Luo L. Small GTPase Cdc42 is required for multiple aspects of dendritic morphogenesis. J Neurosci 2003, 23:3118-3123.
199. Segal M. Dendritic spines and long-term plasticity. Nat Rev Neurosci 2005, 6:277-284.
200. Seidman L.J., Giuliano A.J., Meyer E.C., Addington J., Cadenhead K.S., Cannon T.D., McGlashan T.H., Perkins D.O., Tsuang M.T., Walker E.F., Woods S.W., Bearden C.E., Christensen B.K., Hawkins K., Heaton R., Keefe R.S., Heinssen R., Cornblatt B.A. Neuropsychology of the prodrome to psychosis in the NAPLS consortium: relationship to family history and conversion to psychosis. Arch Gen Psychiatry 2010, 67:578-588.
201. Selemon L.D., Goldman-Rakic P.S. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 1999, 45:17-25.
202. Selemon L.D., Mrzljak J., Kleinman J.E., Herman M.M., Goldman-Rakic P.S. Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. Arch Gen Psychiatry 2003, 60:69-77.
203. Selemon L.D., Rajkowska G., Goldman-Rakic P.S. Abnormally high neuronal density in the schizophrenic cortex: a morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995, 52:805-818.
204. Selemon L.D., Rajkowska G., Goldman-Rakic P.S. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol 1998, 392:402-412.
205. Shao L., Martin M.V., Watson S.J., Schatzberg A., Akil H., Myers R.M., Jones E.G., Bunney W.E., Vawter M.P. Mitochondrial involvement in psychiatric disorders. Ann Med 2008, 40:281-295.
206. Silva-Gomez A.B., Rojas D., Juarez I., Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 2003, 983:128-136.
207. Simon T.J., Ding L., Bish J.P., McDonald-McGinn D.M., Zackai E.H., Gee J. Volumetric, connective, and morphologic changes in the brains of children with chromosome 22q11.2 deletion syndrome: an integrative study. NeuroImage 2005, 25:169-180.
208. Smart F.M., Halpain S. Regulation of dendritic spine stability. Hippocampus 2000, 10:542-554.
209. Sporn A.L., Greenstein D.K., Gogtay N., Jeffries N.O., Lenane M., Gochman P., Clasen L.S., Blumenthal J., Giedd J.N., Rapoport J.L. Progressive brain volume loss during adolescence in childhood-onset schizophrenia. Am J Psychiatry 2003, 160:2181-2189.
210. Steen R.G., Mull C., McClure R., Hamer R.M., Lieberman J.A. Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br J Psychiatry 2006, 188:510-518.
211. Sun D., Phillips L., Velakoulis D., Yung A., McGorry P.D., Wood S.J., Van Erp T.G., Thompson P.M., Toga A.W., Cannon T.D., Pantelis C. Progressive brain structural changes mapped as psychosis develops in 'at risk' individuals. Schizophr Res 2009, 108:85-92.
212. Supprian T., Ulmar G., Bauer M., Schuler M., Puschel K., Retz-Junginger P., Schmitt H.P., Heinsen H. Cerebellar vermis area in schizophrenic patients - a post-mortem study. Schizophr Res 2000, 42:19-28.
213. Sweet R.A., Bergen S.E., Sun Z., Marcsisin M.J., Sampson A.R., Lewis D.A. Anatomical evidence of impaired feedforward auditory processing in schizophrenia. Biol Psychiatry 2007, 61:854-864.
214. Sweet R.A., Bergen S.E., Sun Z., Sampson A.R., Pierri J.N., Lewis D.A. Pyramidal cell size reduction in schizophrenia: evidence for involvement of auditory feedforward circuits. Biol Psychiatry 2004, 55:1128-1137.
215. Sweet R.A., Henteleff R.A., Zhang W., Sampson A.R., Lewis D.A. Reduced dendritic spine density in auditory cortex of subjects with schizophrenia. Neuropsychopharmacology 2009, 34:374-389.
216. Sweet R.A., Pierri J.N., Auh S., Sampson A.R., Lewis D.A. Reduced pyramidal cell somal volume in auditory association cortex of subjects with schizophrenia. Neuropsychopharmacology 2003, 28:599-609.
217. Tada T., Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 2006, 16:95-101.
218. Takahashi T., Wood S.J., Yung A.R., Soulsby B., McGorry P.D., Suzuki M., Kawasaki Y., Phillips L.J., Velakoulis D., Pantelis C. Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. Arch Gen Psychiatry 2009, 66:366-376.
219. Tamminga C.A., Stan A.D., Wagner A.D. The hippocampal formation in schizophrenia. Am J Psychiatry 2010, 167:1178-1193.
220. Tan G.M., Arnone D., McIntosh A.M., Ebmeier K.P. Meta-analysis of magnetic resonance imaging studies in chromosome 22q11.2 deletion syndrome (velocardiofacial syndrome). Schizophr Res 2009, 115:173-181.
221. Tang Y., Janssen W.G., Hao J., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 2004, 14:215-223.
222. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
223. Tsai S.Y., Hayashi T., Harvey B.K., Wang Y., Wu W.W., Shen R.F., Zhang Y., Becker K.G., Hoffer B.J., Su T.P. Sigma-1 receptors regulate hippocampal dendritic spine formation via a free radical-sensitive mechanism involving Rac1xGTP pathway. Proc Natl Acad Sci USA 2009, 106:22468-22473.
224. Uhlhaas P.J., Haenschel C., Nikolic D., Singer W. The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr Bull 2008, 34:927-943.
225. Usall J., Huerta-Ramos E., Iniesta R., Cobo J., Araya S., Roca M., Serrano-Blanco A., Teba F., Ochoa S. Raloxifene as an adjunctive treatment for postmenopausal women with schizophrenia: a double-blind, randomized, placebo-controlled trial. J Clin Psychiatry 2011, 72:1552-1557.
226. Vincent S.L., McSparren J., Wang R.Y., Benes F.M. Evidence for ultrastructural changes in cortical axodendritic synapses following long-term treatment with haloperidol or clozapine. Neuropsychopharmacology 1991, 5(3):147-155.
227. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., Nord A.S., Kusenda M., Malhotra D., Bhandari A., Stray S.M., Rippey C.F., Roccanova P., Makarov V., Lakshmi B., Findling R.L., Sikich L., Stromberg T., Merriman B., Gogtay N., Butler P., Eckstrand K., Noory L., Gochman P., Long R., Chen Z., Davis S., Baker C., Eichler E.E., Meltzer P.S., Nelson S.F., Singleton A.B., Lee M.K., Rapoport J.L., King M.C., Sebat J. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008, 320:539-543.
228. Wang H.D., Deutch A.Y. Dopamine depletion of the prefrontal cortex induces dendritic spine loss: reversal by atypical antipsychotic drug treatment. Neuropsychopharmacology 2008, 33:1276-1286.
229. Wang H.D., Stanwood G.D., Grandy D.K., Deutch A.Y. Dystrophic dendrites in prefrontal cortical pyramidal cells of dopamine D1 and D2 but not D4 receptor knockout mice. Brain Res 2009, 1300:58-64.
230. Wang M., Gamo N.J., Yang Y., Jin L.E., Wang X.J., Laubach M., Mazer J.A., Lee D., Arnsten A.F. Neuronal basis of age-related working memory decline. Nature 2011, 476:210-213.
231. Wang X., Su B., Lee H.G., Li X., Perry G., Smith M.A., Zhu X. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci 2009, 29:9090-9103.
232. Washizuka S., Kametani M., Sasaki T., Tochigi M., Umekage T., Kohda K., Kato T. Association of mitochondrial complex I subunit gene NDUFV2 at 18p11 with schizophrenia in the Japanese population. Am J Med Genet B Neuropsychiatr Genet 2006, 141B:301-304.
233. Weickert C.S., Straub R.E., McClintock B.W., Matsumoto M., Hashimoto R., Hyde T.M., Herman M.M., Weinberger D.R., Kleinman J.E. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch Gen Psychiatry 2004, 61:544-555.
234. Williams R.S., Ferrante R.J., Caviness V.S. The Golgi rapid method in clinical neuropathology: the morphologic consequences of suboptimal fixation. J Neuropatho Exp Neurol 1978, 37:13-33.
235. Wilson C.J. GABAergic inhibition in the neostriatum. Prog Brain Res 2007, 160:91-110.
236. Wu E.Q., Birnbaum H.G., Shi L., Ball D.E., Kessler R.C., Moulis M., Aggarwal J. The economic burden of schizophrenia in the United States in 2002. J Clin Psychiatry 2005, 66:1122-1129.
237. Xie Z., Cahill M.E., Penzes P. Kalirin loss results in cortical morphological alterations. Mol Cell Neurosci 2010, 43:81-89.
238. Yoshida T., McCarley R.W., Nakamura M., Lee K., Koo M.S., Bouix S., Salisbury D.F., Morra L., Shenton M.E., Niznikiewicz M.A. A prospective longitudinal volumetric MRI study of superior temporal gyrus gray matter and amygdala-hippocampal complex in chronic schizophrenia. Schizophr Res 2009, 113:84-94.
239. Young K.A., Holcomb L.A., Yazdani U., Hicks P.B., German D.C. Elevated neuron number in the limbic thalamus in major depression. Am J Psychiatry 2004, 161:1270-1277.
240. Young K.A., Manaye K.F., Liang C.-L., Hicks P.B., German D.C. Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol Psychiatry 2000, 47:944-953.
241. Yuste R. Dendritic spines and distributed circuits. Neuron 2011, 71:772-781.
242. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089.
243. Zhang W., Benson D.L. Development and molecular organization of dendritic spines and their synapses. Hippocampus 2000, 10:512-526.