Studies on the hippocampal formation: From basic development to clinical applications: Studies on schizophrenia

Progress in Neurobiology

Volumn 90, Issue 2, 2010, Pages 263-275

  Freedman, Robert ^a   Goldowitz, Dan ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Alpha 7 nicotinic acetylcholine receptor; Dentate gyrus; Development; Hippocampus; In oculo transplantation; Schizophrenia

Indexed keywords

3 (2,4 DIMETHOXYBENZYLIDENE)ANABASEINE; BUNGAROTOXIN RECEPTOR; CHOLINE; DOPAMINE RECEPTOR BLOCKING AGENT; NEUROLEPTIC AGENT; NICOTINE; PLACEBO;

BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN FUNCTION; CLINICAL TRIAL; COGNITION; DENTATE GYRUS; DEVELOPMENTAL DISORDER; DOPAMINERGIC TRANSMISSION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG TARGETING; FAMILY HISTORY; GENETIC LINKAGE; HIPPOCAMPUS; HUMAN; INNERVATION; INTERNEURON; MEMORY DISORDER; MESENCEPHALON; NERVE CELL LESION; NERVE STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NEUROMODULATION; NONHUMAN; NORADRENERGIC NERVE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SCHIZOPHRENIA; SENSORY DYSFUNCTION;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; HIPPOCAMPUS; HUMANS; NEURAL INHIBITION; RECEPTORS, NICOTINIC; SCHIZOPHRENIA;

EID: 76849087246     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2009.10.008     Document Type: Review

References (87)

1. Adams C.E. Comparison of alpha7 nicotinic acetylcholine receptor development in the hippocampal formation of C3H and DBA/2 mice. Dev. Brain Res. 143 (2003) 137-149
2. Adams C.E., Broide R.S., Chen Y., Winzer-Serhan U.H., Henderson T.A., Leslie F.M., and Freedman R. Development of the alpha7 nicotinic cholinergic receptor in rat hippocampal formation. Dev. Brain Res. 139 2 (2002) 175-187
3. Adams C.E., and Freedman R. Nicotinic antagonist α-bungarotoxin binding to rat hippocampal neurons containing nitric oxide synthase (NOS). Brain Res. 776 (1997) 111-116
4. Adams C.E., Stitzel J.A., Collins A.C., and Freedman R. Alpha7-Nicotinic receptor expression and the anatomical organization of hippocampal interneurons. Brain Res. 922 2 (2001) 180-190
5. Adler L.E., Hoffer L.D., Wiser A., and Freedman R. Normalization of auditory physiology by cigarette smoking in schizophrenic patients. Am. J. Psychiatry 150 (1993) 1856-1861
6. Adler L.E., Pachtman E., Franks R., and Freedman R. Neurophysiologic evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biol. Psychiatry 17 (1982) 639-654
7. Akbarian S., Vinuela A., Kim J.J., Potkin S.G., Bunney Jr. W.E., and Jones E.G. Distorted distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch. Gen. Psychiatry 50 (1993) 178-187
8. Albright C.D., Tsai A.Y., Friedrich C.B., Mar M.H., and Zeisel S.H. Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Res.: Dev. Brain Res. 113 (1999) 13-20
9. Alkondon M., and Albuquerque E.X. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J. Pharmacol. Exp. Ther. 265 (1993) 1455-1473
10. Alkondon M., Pereira E.F.R., Cortes W.S., Maelicke A., and Albuquerque E.X. Choline is a selective agonist at alpha7 nicotinic acetylcholine receptors in rat brain neurons. Eur. J. Neurosci. 9 (1997) 2734-2742
11. Aramakis V.B., Hsieh C.Y., Leslie F.M., and Metherate R. A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex. J. Neurosci. 20 (2000) 6106-6116
12. Ayer-LeLievre C., Olson L., Ebendal T., Seiger A., and Persson H. Expression of the betanerve growth factor gene in hippocampal neurons. Science 240 (1988) 1339-1341
13. Bickford-Wimer P.C., Nagamoto H., Johnson R., Adler L.E., Egan M., Rose G.M., and Freedman R. Auditory sensory gating in hippocampal neurons: a model system in the rat. Biol. Psychiatry 27 (1990) 183-192
14. Björklund H., Seiger A., Hoffer B., and Olson L. Trophic effects of brain areas on the developing cerebral cortex: I. Growth and histological organization of intraocular grafts. Brain Res. 282 2 (1983) 131-140
15. Bleuler, E. 1950. Dementia Praecox oder Gruppe der Schizophrenien. Leipzig, Deuticke, 1911. English version: Demenia Praecox or the Group of Schizophrenias. New York, International Universities Press.
16. Boutros N.N., and Kwan S.W. Test-retest reliability of the rat N40 auditory evoked response: preliminary data. Psychiatry Res. 81 2 (1998) 269-276
17. 125I]-α-bungarotoxin binding in human postmortem brain. J. Comp. Neurol. 387 (1997) 385-398
18. Broadbent D. Perception and Communication (1958), Pergamon, Oxford, England
19. Brockhaus-Dumke A., Schultze-Lutter F., Mueller R., Tendolkar I., Bechdolf A., Purkop P., Klosterkoetter J., and Ruhmann R. Sensory gating in schizophrenia: P50 and N100 gating in antipsychotic-free subjects at risk, first-episode, and chronic patients. Biol. Psychiatry 64 (2008) 376-384
20. Browning M.D., Dudek E.M., Rapier J.L., Leonard S., and Freedman R. Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics. Biol. Psychiatry 34 (1993) 529-535
21. Cadenhead K.S., Light G.A., Geyer M.A., and Braff D.L. Sensory gating deficits assessed by the P50 event-related potential in subjects with schizotypal personality disorder. Am. J. Psychiatry 157 (2000) 55-59
22. Court J.A., Lloyd S., Johnson M., Griffiths M., Birdsall N.J.M., Piggott M.A., Oakley A.E., Ince P.G., Perry E.K., and Perry R.H. Nicotinic and muscarinic cholinergic receptor binding in the human hippocampal formation during development and aging. Dev. Brain Res. 101 (1997) 93-105
23. Court J., Spurden D., Lloyd S., McKeith I., Ballard C., Cairns N., Kerwin R., Perry R., and Perry E. Neuronal nicotinic receptors in dementia with Lewy bodies and schizophrenia: alpha-bungarotoxin and nicotine binding in the thalamus. J. Neurochem. 73 (1999) 1590-1597
24. De Fiebre C.M., Meyer E.M., Henry J.C., Muraskin S.I., Kem W.R., and Papke R.L. Characterization of a series of anabaseine-derived compounds reveals that the 3-(4)-dimethylaminocinnamylidine derivative is a selective agonist at neuronal nicotinic alpha-7/125 I-alpha-bungarotoxin receptor subtypes. Mol. Pharmacol. 47 (1995) 164-171
25. Dempster E.L., Toulopoulou T., McDonald C., Bramon B., Walshe M., Wickham H.P., Sham P.C., Murray R.M., and Collier D.A. Episodic memory performance predicted by the 2bp deletion in exon 6 of the "Alpha 7-Like" nicotinic receptor subunit gene. Am. J. Psychiatry 163 (2006) 1832-1834
26. Ferrier I.N., Roberts G.W., Crow T.J., Johnstone E.C., Owens D.G., Lee Y.C., O'Shaughnessy D., Adrian T.E., Polak J.M., and Bloom S.R. Reduced cholecystokinin-like and somatostatin-like immunoreactivity in limbic lobe is associated with negative symptoms in schizophrenia. Life Sci. 33 (1983) 475-482
27. Frazier C.J., Rollins Y.D., Breese C.R., Leonard S., Freedman R., and Dunwiddie T.V. Acetylcholine activates an α-bungarotoxin sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J. Neurosci. 18 (1998) 1187-1195
28. Freedman R., Adler L.E., Bickford P., Byerley W., Coon H., Cullum C.M., Griffith J.M., Harris J.G., Leonard S., and Miller C. Schizophrenia and nicotinic receptors. Harvard Rev. Psychiatry 2 (1994) 179-192
29. Freedman R., Coon H., Myles-Worsley M., Orr-Urtreger A., Olincy A., Davis A., Polymeropoulos M., Holik J., Hopkins J., Hoff M., Rosenthal J., Waldo M.C., Reimherr F., Wender P., Yaw J., Young D.A., Breese C.R., Adams C., Patterson D., Adler L.E., Kruglyak L., Leonard S., and Byerley W. Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 587-592
30. Freedman R., Olincy A., Buchanan R.W., Harris J.G., Gold J.M., Johnson L., Allensworth D., Guzman-Bonilla A., Clement B., Ball M.P., Kutnick J., Pender V., Martin L.F., Stevens K.E., Wagner B.D., Zerbe G.O., Soti F., and Kem W.R. Initial phase 2 trial of a nicotinic agonist in schizophrenia. Am. J. Psychiatry 165 (2008) 1040-1047
31. Freedman R., Stromberg I., Nordstrom A.L., Seiger A., Olson L., Bygdeman M., Wiesel F.A., Granholm A.C., and Hoffer B.J. Neuronal development in embryonic brain tissue derived from schizophrenic women and grafted to animal hosts. Schizophr. Res. 13 (1994) 259-270
32. Freedman R., Wetmore C., Stromberg I., Leonard S., and Olson L. a-Bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J. Neurosci. 13 5 (1993) 1965-1975
33. Garcia-Rill E., Buchanan R., McKeon K., Skinner R.D., and Wallace T. Smoking during pregnancy: postnatal effects on arousal and attentional brain systems. Neurotoxicology 28 5 (2007) 915-923
34. Gejman P.V., Sanders A.R., Badner J.A., Qiuhe C., and Jing Z. Linkage analysis of schizophrenia to chromosome 15. Am. J. Med. Genet. 105 8 (2001) 789-793
35. Goldowitz D., Seiger A., and Olson L. Degree of hyperinnervation of area dentata by locus coeruleus in the presence of septum or entorhinal cortex as studied by sequential intraocular triple transplantation. Exp. Brain Res. 56 (1984) 351-360
36. Goldowitz D., Seiger A., and Olson L. Regulation of axonal ingrowth into area dentata as studied by sequential, double intraocular brain tissue transplantation. J. Comp. Neurol. 227 (1984) 50-62
37. Goldowitz D., Seiger A., and Olson L. Anatomy of the isolated area dentata grown in the rat anterior eye. J. Comp. Neurol. 208 (1982) 382-400
38. Gossell-Williams M., Fletcher H., McFarlane-Anderson N., Jacob A., and Zeisel S. Dietary intake of choline and plasma choline concentrations in pregnant women in Jamaica. West Indian Med. J. 54 (2005) 355-359
39. Greenwood T.A. The Consortium on the genetics of schizophrenia. Soc. Biol. Psychiatry (2008) Abstract 247
40. Guan Z.Z., Zhang X., Biennow K., and Nordberg A. Decreased protein level of nicotinic receptor [alpha]7 subunit in the frontal cortex from schizophrenic brain. Neurochemistry 8 (1998) 1779-1782
41. Hall M.H., Rijsdijk F., Picchioni M., Schulze K., Ettinger U., Toulopoulou T., Bramon E., Murray R.M., and Sham P. Substantial shared genetic influences on schizophrenia and event-related potentials. Am. J. Psychiatry 164 5 (2007) 804-812
42. Hong L.E., Summerfelt A., McMahon R.P., Thaker G.K., and Buchanan R.W. Gamma/beta oscillation and sensory gating deficit in schizophrenia. NeuroReport 15 (2004) 155-159
43. Hong L.E., Summerfelt A., Mitchell B.D., McMahon R.P., Wonodi I., Buchanan R.W., and Thaker G.K. Sensory gating endophenotype based on its neural oscillatory pattern and heritability estimate. Arch. Gen. Psychiatry 65 (2008) 977-1104
44. Ilcol Y.O., Uncu G., and Ulus I.H. Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery, and in newborns. Arch. Physiol. Biochem. 110 (2002) 393-399
45. Iritani S., Kuroki N., Niizato K., and Ikeda K. Morphological changes in neuropeptide Y-positive fiber in the hippocampal formation of schizophrenics. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 24 (2000) 241-249
46. Javitt D.C., Jayachandra M., Lindsley R.W., Specht C.M., and Schroeder C.E. Schizophrenia-like deficits in auditory P1 and N1 refractoriness induced by the psychomimetic agent phencyclidine (PCP). Clin. Neurophysiol. 111 5 (2000) 833-836
47. Judd L., McAdams L., Budnick B., and Braff D.L. Sensory gating deficits in schizophrenia: new results. Am. J. Psychiatry 149 (1992) 488-493
48. Kaufmann C.A., Suarez B., Malaspina D., Pepple J., Svrakic D., Markel P.D., Meyer J., Zambuto C.T., Schmitt K., Matise T.C., Harkavy Friedman J.M., Hampe C., Lee H., Shore D., Wynne D., Faraone S.V., Tsuang M.T., and Cloninger C.R. NIMH genetics initiative millennium schizophrenia consortium: linkage analysis of African-American pedigrees. Am. J. Med. Genet. 81 4 (1998) 282-289
49. Leonard S., Gault J., Hopkins J., Logel J., Vianzon R., Short M., Drebing C., Berger G., Venn D., Sirota P., Zerbe G., Olincy A., Ross R.G., Adler L.E., and Freedman R. Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia. Arch. Gen. Psychiatry 59 (2002) 1085-1096
50. Liu C.M., Hwu H.G., Lin M.W., Ou-Yang W.C., Lee S.F.C., Fann C.S.J., Wong S.H., and Hsieh S.H. Suggestive evidence for linkage of schizophrenia to markers at chromosome 15q13-14 in Taiwanese families. Am. J. Med. Genet. 105 (2001) 658-661
51. Liu Y., Zhang H., Ju G., Zhang X., Xu Q., Liu S., Yu Y., Shi J., Boyle S., Wang Z., Shen Y., and Wie J. A study of the PEMT gene in schizophrenia. Neurosci. Lett. 424 (2007) 203-206
52. Liu Z., Neff R.A., and Berg D.K. Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 314 (2006) 1610-1613
53. Luntz-Leybman V., Bickford P.C., and Freedman R. Cholinergic gating of response to auditory stimuli in rat hippocampus. Brain Res. 587 (1992) 130-136
54. Louchart-de la Chapelle S., Nkam I., Houy E., Belmont A., Menard J.F., Roussignol A.C., Siwek O., Mezerai M., Guillermou M., Levillain D., Dollfus S., Campion D., and Thibaut F. A concordance study of three electrophysiological measures in schizophrenia. Am. J. Psychiatry 162 (2005) 466-474
55. Malaspina D., Storer S., Furman V., Esser P., Printz D., Berman A., Lignelli A., Gorman J., and Van Heertum R. SPECT study of visual fixation in schizophrenia and comparison subjects. Biol. Psychiatry 46 1 (1999) 89-93
56. Marutle A., Zhang X., Court J., Piggot M., Johnson M., Perry R., Perry E., and Nordberg A. Laminar distribution of nicotinic receptor subtypes in cortical regions in schizophrenia. J. Chem. Neuroanat. 22 (2001) 115-126
57. Martin L.A., Tan S.S., and Goldowitz D. Clonal architecture of the mouse hippocampus. J. Neurosci. 22 9 (2002) 3520-3530
58. Maxwell C.R., Liang Y., Kelly M.P., Kanes S.J., Abel T., and Siegel S.J. Mice expressing constitutively active Gsalpha exhibit stimulus encoding deficits similar to those observed in schizophrenia patients. Neuroscience 141 3 (2006) 1257-1264
59. Meck W.H., Smith R.A., and Williams C.L. Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behav. Neurosci. 103 (1989) 1234-1241
60. Nagy J.I., Price M.L., Staines W.A., Lynn B.D., and Granholm A.C. The hyaluronan receptor RHAMM in noradrenergic fibers contributes to axon growth capacity of locus coeruleus neurons in an intraocular transplant model. Neuroscience 86 1 (1998) 241-255
61. Olincy A., Harris J.G., Johnson L.L., Pender V., Kongs S., Allensworth D., Ellis J., Zerbe G.O., Leonard S., Stevens K.E., Stevens J.O., Martin L., Adler L.E., Soti F., Kem W.R., and Freedman R. Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch. Gen. Psychiatry 63 (2006) 630-638
62. Olson L., Seiger A., Taylor D., Freedman R., and Hoffer B.J. Conditions for adrenergic hyperinnervation in hippocampus: I. Histochemical evidence from intraocular double grafts. Exp. Brain Res. 39 (1980) 277-288
63. Patterson J.V., Hetrick W.P., Boutros N.N., Jin Y., Sandman C., Stern H., Potkin S., and Bunney Jr. W.E. P50 sensory gating ratios in schizophrenics and controls: a review and data analysis. Psychiatry Res. 158 2 (2008) 226-247
64. Porter R.H., Eastwood S.L., and Harrison P.J. Distribution of kainate receptor subunit mRNAs in human hippocampus, neocortex and cerebellum, and bilateral reduction of hippocampal GluR6 and KA2 transcripts in schizophrenia. Brain Res. 751 (1997) 217-231
65. Price G.W., Michie P.T., Johnston J., Innes-Brown H., Kent A., Clissa P., and Jablensky A.V. A multivariate electrophysiological endophenotype from a unitary cohort, shows greater research utility than any single feature in the western Australian family study of schizophrenia. Biol. Psychiatry 60 1-10 (2005) 2005
66. Radek R.J., Miner H.M., Bratcher N.A., Decker M.W., Gopalakrishnan M., and Bitner R.S. Alpha4beta2 nicotinic receptor stimulation contributes to the effects of nicotine in the DBA/2 mouse model of sensory gating. Psychopharmacology 187 1 (2006) 47-55
67. Raux G., Bonnet-Brilhault F., Louchart S., Houye E., Gantier R., Levillain D., Allio G., Haouzir S., Petit M., and Martinez M. The -2bp deletion in exon 6 of the alpha 7-like nicotinic receptor subunit gene is a risk factor for the P50 sensory gating deficit. Mol. Psych. 7 (2002) 1006-1011
68. Riley B.P., Makoff A., Mogudi-Carter M., Jenkins T., Williamson R., Collier D., and Murray R. Haplotype transmission disequilibrium and evidence for linkage of the CHRNA7 gene region to schizophrenia in Southern African Bantu families. Am. J. Med. Genet. 96 (2000) 196-201
69. Sanders A.R., Duan J., Levinson D.F., Shi J., He D., Hou C., Burrell G.J., Rice J.P., Nertney D.A., Olincy A., Roznic P., Vinogradov S., Buccola N.G., Mowry B.J., Freedman R., Amin F., Black D.W., Silverman J.M., Byerley W.F., Crowe R.R., Cloninger C.R., Martinez M., and Gejman P.V. No significant association of 14 candidate genes with schizophrenia in a large European ancestry sample: implications for psychiatric genetics. Am. J. Psychiatry 164 (2008) 497-506
70. Seguela P., Wadiche J., Dineley-Miller K., Dani J.A., and Patrick J.W. Molecular cloning, functional properties and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13 (1993) 596-604
71. Siegel C., Waldo M., Mizner G., Adler L.E., and Freedman R. Deficits in sensory gating in schizophrenic patients and their relatives. Arch. Gen. Psychiatry 41 (1984) 607-612
72. Simpson M.D., Slater P., Deakin J.F., Royston M.C., and Skan W.J. Reduced GABA uptake sites in the temporal lobe in schizophrenia. Neurosci. Lett. 107 (1989) 211-215
73. Stassen H.H., Bridler R., Hagele S., Hergerberg M., Mehmann B., Schinzel A., and Scharfetter C. Schizophrenia and smoking: evidence for a common neurobiological basis?. Am. J. Med. Genet. 96 2 (2000) 173-177
74. Stefansson H., Rujescu D., Cichon S., Ingason A., Steinberg S., Fossdal R., Sigurdsson E., Sigmundsson T., Buizer-Voskamp J.E., Hansen T., Jakobsen K.D., Muglia P., Francks C., Matthews P.M., Gylfasson A., Halldorsson B.V., Gudbjartsson D., Thorgeirsson T.E., Sigudsson A., Jonasdottir A., Jonasdottir A., Bjornsson A., Mattiasdottir S., Blondal T., Haraldsson M., Magnusdottir B.B., Giegling I., Moller H.J., Hartmann A., Shianna K.V., Ge D., Need A.C., Crombie C., Fraser G., Walker N., Lonnqvist J., Suvisaari J., Tuulio-Hendriksson A., Paunio T., Toulopoulou T., Bramon E., Di Forti M., Murray R., Ruggeri M., Vassos E., Tosato S., Walshe M., Li T., Vasilescu C., Muhleisen T.W., Wang A.G., Ullum H., Djurovic S., Melle I., Olesen J., Kiemeney L.A., Franke B., Sabatti C., Freimer N.B., Gulcher J.R., Thorsteinsdottir U., Kong A., Andreassen O.A., Ophoff R.A., Georgi A., Rietschel M., Werge T., Petursson H., Goldstein D.B., Nothen M.M., Peltonen L., Collier D.A., St Clair D., and Stefansson K. Large recurrent microdeletions associated with schizophrenia. Nature 455 (2008) 232-236
75. Stevens K.E., Adams C., Yonchek J., Hickel C., Danielson J., and Kisley M. Permanent improvement in deficient sensory inhibition in DBA/2 mice with increased perinatal choline. Psychopharmacology 198 (2008) 413-420
76. Stevens K.E., Freedman R., Collins A.C., Hall M., Leonard S., Marks M.J., and Rose G.M. Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin-binding nicotinic cholinergic receptors in inbred mouse strains. Neuropsychopharmacology 15 (1996) 152-162
77. Stevens K.E., Kem W.R., Mahnir V.M., and Freedman R. Selective α7-nicotinic agonists normalize inhibition of auditory response in DBA mice. Psychopharmacology 126 (1998) 320-327
78. Stone J. International schizophrenia consortium. Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455 (2008) 237-241
79. Thoma R.J., Hanlon F.M., Moses S.N., Edgar J.C., Huang M., Weisend M.P., Irwin J., Sherwood A., Paulson K., Bustillo J., Alder L.E., Miller G.A., and Canive J.M. Lateralization of auditory sensory gating and neuropsychological dysfunction in schizophrenia. Am. J. Psychiatry 160 (2003) 1595-1605
80. Tsuang D.W., Skol A.D., Faraone S.V., Bingham S., Young K.A., Prabhudesai S., Haverstock S.L., Mena F., Menon A.S., Bisset D., Pepple J., Sauter F., Baldwin C., Weiss D., Collins J., Boehnke M., Schellenberg G.D., and Tsuang M.T. Examination of genetic linkage of chromosome 15 to schizophrenia in a large veterans affairs cooperative study sample. Am. J. Med. Genet. 105 (2001) 662-668
81. Vawter M.P., Thatcher L., Usen N., Hyde T.M., Kleinman J.E., and Freed W.J. Reduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia. Mol. Psychiatry 7 (2002) 571-578
82. Venables P.H. Input dysfunction in schizophrenia. Prog. Exp. Person. Res. 72 (1964) 1-47
83. Willis L., Quintero E.M., and Nelson M. Granholm ACh. Regulation of trophic factor expression by innervating target regions in intraocular double transplants. Cell Transplant. 14 1 (2005) 21-29
84. Xu J., Pato M.T., Dalla Torre C., Medeiros H., Carvalho C., Basile V.S., Bauer A., Dourado A., Valente J., Soares M.J., Macedo A.A., Coelho I., Ferreira C.P., Azevedo M.H., Macciardi F., Kennedy J.L., and Pato C.N. Evidence of linkage disequilibrium between the alpha 7-nicotinic receptor gene (CHRNA7) locus and schizophrenia in Azorean Families. Am. J. Med. Genet. 105 (2001) 669-674
85. Yee C.M., Nuechterlein K.H., Morris S.E., and White P.M. P50 suppression in recent-onset schizophrenia: clinical correlates and risperidone effects. J. Abnorm. Psychol. 107 4 (1998) 691-698
86. Zeisel S.H. The fetal origins of memory: the role of dietary choline in optimal brain development. J. Pediatr. 149 (2006) S131-S136
87. Zilles K., Wu J., Crusio W.E., and Schwegler H. Water maze and radial maze learning and the density of binding sites of glutamate, GABA, and serotonin receptors in the hippocampus of inbred mouse strains. Hippocampus 10 (2000) 213-225