Targeting the hippocampal mossy fiber synapse for the treatment of psychiatric disorders

Molecular Neurobiology

Volumn 39, Issue 1, 2009, Pages 24-36

  Kobayashi, Katsunori ^a,b  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Antidepressant; Dentate gyrus; Hippocampus; Mossy fiber; Neuronal maturation; Psychiatric disorder; Schizophrenia

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; BUNGAROTOXIN RECEPTOR AGONIST; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; FLUOXETINE; HALOPERIDOL; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; MONOAMINE OXIDASE INHIBITOR; NEUROLEPTIC AGENT; NICOTINIC AGENT; PHOSPHODIESTERASE INHIBITOR; SEROTONIN UPTAKE INHIBITOR; TRICYCLIC ANTIDEPRESSANT AGENT; UNCLASSIFIED DRUG; VASOPRESSIN RECEPTOR ANTAGONIST; VASOPRESSIN V1B RECEPTOR;

DENTATE GYRUS; DEPRESSION; DRUG EFFECT; DRUG TARGETING; ELECTROCONVULSIVE THERAPY; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; MENTAL DISEASE; MOSSY FIBER; NERVE CELL; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PYRAMIDAL NERVE CELL; REVIEW; SCHIZOPHRENIA; SYNAPSE; ANIMAL; CYTOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTIPSYCHOTIC AGENTS; DENTATE GYRUS; HUMANS; MENTAL DISORDERS; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; SYNAPSES;

EID: 63149107984     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-008-8049-5     Document Type: Review

References (196)

1. SM Lawrie SS Abukmeil 1998 Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies Br J Psychiatry 172 110 120 (Pubitemid 28097708)
2. P Videbech B Ravnkilde 2004 Hippocampal volume and depression: a meta-analysis of MRI studies Am J Psychiatry 161 1957 1966 (Pubitemid 39441394)
3. RG Steen C Mull R McClure RM Hamer JA Lieberman 2006 Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies Br J Psychiatry 188 510 518 (Pubitemid 43844097)
4. SS Shergill MJ Brammer SCR Williams RM Murray PK McGuire 2000 Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging Arch Gen Psychiatry 57 1033 1038 (Pubitemid 30818871)
5. V Oertel A Rotarska-Jagiela VG van de Ven C Haenschel K Maurer DEJ Linden 2007 Visual hallucinations in schizophrenia investigated with functional magnetic resonance imaging Psychiatry Res 156 269 273 (Pubitemid 350116559)
6. K Takao N Yamasaki T Miyakawa 2007 Impact of brain-behavior phenotypying of genetically-engineered mice on research of neuropsychiatric disorders Neurosci Res 58 124 132 (Pubitemid 46843324)
7. H Zeng S Chattarji M Barbarosie L Rondi-Reig BD Philpot T Miyakawa MF Bear S Tonegawa 2001 Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory Cell 107 617 629 (Pubitemid 34014863)
8. T Miyakawa LM Leiter DJ Gerber RR Gainetdinov TD Sotnikova H Zeng MG Caron S Tonegawa 2003 Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia Proc Natl Acad Sci USA 100 8987 8992 (Pubitemid 36899210)
9. DJ Gerber D Hall T Miyakawa S Demars JA Gogos M Karayiorgou S Tonegawa 2003 Evidence for association of schizophrenia with genetic variation in the 8p21.3 gene, PPP3CC, encoding the calcineurin gamma subunit Proc Natl Acad Sci USA 100 8993 8998 (Pubitemid 36899211)
10. Y Horiuchi H Ishiguro M Koga T Inada N Iwata N Ozaki H Ujike T Muratake T Someya T Arinami 2007 Support for association of the PPP3CC gene with schizophrenia Mol Psychiatry 12 891 893 (Pubitemid 47482698)
11. YL Liu CSJ Fann CM Liu CC Chang WC Yang SI Hung SL Yu TJ Hwang MH Hsieh CC Liu MM Tsuang JY Wu YS Jou SV Faraone MT Tsuang WJ Chen H-G Hwu 2007 More evidence supports the association of PPP3CC with schizophrenia Mol Psychiatry 12 966 974 (Pubitemid 47482692)
12. RC O'Reilly JL McClelland 1994 Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off Hippocampus 4 661 682
13. RP Kesner PE Gilbert GV Wallenstein 2000 Testing neural network models of memory with behavioral experiments Curr Opin Neurobiol 10 260 265 (Pubitemid 30201121)
14. PE Gilbert RP Kesner I Lee 2001 Dissociating hippocampal subregions: a double dissociation between dentate gyrus and CA1 Hippocampus 11 626 636 (Pubitemid 34065491)
15. JK Leutgeb S Leutgeb M-B Moser EI Moser 2007 Pattern separation in the dentate gyrus and CA3 of the hippocampus Science 315 961 966 (Pubitemid 46281178)
16. MW Jung BL McNaughton 1993 Spatial selectivity of unit activity in the hippocampal granular layer Hippocampus 3 165 182 (Pubitemid 23130073)
17. X-S Liu S Tilwalli G-l Ye PA Lio JF Pasternak BL Trommer 2000 Morphologic and electrophysiologic maturation in developing dentate gyrus granule cells Brain Res 856 202 212 (Pubitemid 30085527)
18. P Ambrogini D Lattanzi S Ciuffoli D Agostini L Bertini V Stocchi S Santi R Cuppini 2004 Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus Brain Res 1017 21 31 (Pubitemid 38917139)
19. C Schmidt-Hieber P Jonas J Bischofberger 2004 Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus Nature 429 184 187 (Pubitemid 38656194)
20. N Yamasaki M Maekawa K Kobayashi Y Kajii J Maeda M Soma K Takao K Tanda K Ohira K Toyama K Kanzaki K Fukunaga Y Sudo H Ichinose M Ikeda N Iwata N Ozaki H Suzuki M Higuchi T Suhara S Yuasa T Miyakawa 2008 Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders Mol Brain 1 6
21. DG Amaral JA Dent 1981 Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions J Comp Neurol 195 51 86 (Pubitemid 11098807)
22. BL McNaughton RGM Morris 1987 Hippocampal synaptic enhancement and information storage within a distributed memory system Trends Neurosci 10 408 415 (Pubitemid 17149102)
23. Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, New York, pp 95-135
24. K Kobayashi T Manabe T Takahashi 1996 Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse Science 273 648 650 (Pubitemid 26262118)
25. PA Salin M Scanziani RC Malenka RA Nicoll 1996 Distinct short-term plasticity at two excitatory synapses in the hippocampus Proc Natl Acad Sci USA 93 13304 13309 (Pubitemid 26382811)
26. F Mori-Kawakami K Kobayashi T Takahashi 2003 Developmental decrease in synaptic facilitation at the mouse hippocampal mossy fibre synapse J Physiol 553 37 48 (Pubitemid 37483914)
27. C Marchal C Mulle 2004 Postnatal maturation of mossy fibre excitatory transmission in mouse CA3 pyramidal cells: a potential role for kainate receptors J Physiol 561 27 37 (Pubitemid 39549464)
28. RS Zucker WG Regehr 2002 Short-term synaptic plasticity Annu Rev Physiol 64 355 405 (Pubitemid 34259234)
29. DA Henze L Wittner G Buzsáki 2002 Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo Nat Neurosci 5 790 795 (Pubitemid 34827598)
30. K Kobayashi M-m Poo 2004 Spike train timing-dependent associative modification of hippocampal CA3 recurrent synapses by mossy fibers Neuron 41 445 454 (Pubitemid 38221046)
31. BJ Claiborne DG Amaral WM Cowan 1986 A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus J Comp Neurol 246 435 458 (Pubitemid 16079508)
32. HE Scharfman DD Kunkel PA Schwartzkroin 1990 Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections Neuroscience 37 693 707 (Pubitemid 20282208)
33. DG Amaral 1978 A Golgi study of cell types in the hilar region of the hippocampus in the rat J Comp Neurol 182 851 914 (Pubitemid 9041117)
34. HE Scharfman 1995 Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons J Neurophysiol 74 179 194
35. M Lysetskiy C Földy I Soltesz 2005 Long- and short-term plasticity at mossy fiber synapses on mossy cells in the rat dentate gyrus Hippocampus 15 691 696 (Pubitemid 41300819)
36. RC Malenka RA Nicoll 1993 NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms Trends Neurosci 16 521 527 (Pubitemid 23341961)
37. EW Harris CW Cotman 1986 Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl D-aspartate antagonists Neurosci Lett 70 132 137 (Pubitemid 16023252)
38. RA Zalutsky RA Nicoll 1990 Comparison of two forms of long-term potentiation in single hippocampal neurons Science 248 1619 1624
39. I Ito H Sugiyama 1991 Roles of glutamate receptors in long-term potentiation at hippocampal mossy fiber synapses Neuroreport 2 333 336
40. 2+channels in hippocampal mossy fiber synaptic transmission and long-term potentiation Neuron 12 261 269
41. D Jaffe D Johnston 1990 Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule J Neurophysiol 64 948 960 (Pubitemid 20319455)
42. NN Urban G Barrionuevo 1996 Induction of Hebbian and non-Hebbian mossy fiber long-term potentiation by distinct patterns of high-frequency stimulation J Neurosci 16 4293 4299 (Pubitemid 26192424)
43. MF Yeckel A Kapur D Johnston 1999 Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism Nat Neurosci 2 625 633 (Pubitemid 30491213)
44. T Tzounopoulos R Janz TC Südhof RA Nicoll RC Malenka 1998 A role for cAMP in long-term depression at hippocampal mossy fiber synapses Neuron 21 837 845 (Pubitemid 28498791)
45. S Lei KA Pelkey L Topolnik P Congar J-C Lacaille CJ McBain 2003 Depolarization-induced long-term depression at hippocampal mossy fiber-CA3 pyramidal neuron synapses J Neurosci 23 9786 9795 (Pubitemid 37371591)
46. M Yokoi K Kobayashi T Manabe T Takahashi I Sakaguchi G Katsuura R Shigemoto H Ohishi S Nomura K Nakamura K Nakao M Katsuki S Nakanishi 1996 Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2 Science 273 645 647 (Pubitemid 26262117)
47. M Scanziani PA Salin KE Vogt RC Malenka RA Nicoll 1997 Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors Nature 385 630 634 (Pubitemid 27087575)
48. D Schmitz J Mellor RA Nicoll 2001 Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses Science 291 1972 1976 (Pubitemid 32216999)
49. RA Nicoll D Schmitz 2005 Synaptic plasticity at hippocampal mossy fibre synapses Nat Rev Neurosci 6 863 876 (Pubitemid 41568728)
50. MG Weisskopf RA Zalutsky RA Nicoll 1993 The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation Nature 362 423 427
51. JM Harrison RG Allen MJ Pellegrino JT Williams OJ Manzoni 2002 Chronic morphine treatment alters endogenous opioid control of hippocampal mossy fiber synaptic transmission J Neurophysiol 87 2464 2470 (Pubitemid 34670717)
52. KA Moore RA Nicoll D Schmitz 2003 Adenosine gates synaptic plasticity at hippocampal mossy fiber synapses Proc Natl Acad Sci USA 100 14397 14402 (Pubitemid 37499248)
53. M Kukley M Schwan BB Fredholm D Dietrich 2005 The role of extracellular adenosine in regulating mossy fiber synaptic plasticity J Neurosci 25 2832 2837 (Pubitemid 40389241)
54. TV Dunwiddie SA Masino 2001 The role and regulation of adenosine in the central nervous system Annu Rev Neurosci 24 31 55 (Pubitemid 32695222)
55. H Alle JRP Geiger 2006 Combined analog and action potential coding in hippocampal mossy fibers Science 311 1290 1293 (Pubitemid 43334719)
56. Z Nusser I Mody 2002 Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells J Neurophysiol 87 2624 2628 (Pubitemid 34670732)
57. K Kobayashi Y Ikeda H Suzuki 2006 Locomotor activity correlates with modifications of hippocampal mossy fibre synaptic transmission Eur J Neurosci 24 1867 1873 (Pubitemid 44583471)
58. K Kobayashi H Suzuki 2007 Dopamine selectively potentiates hippocampal mossy fiber to CA3 synaptic transmission Neuropharmacology 52 552 561 (Pubitemid 46123372)
59. K Kobayashi Y Ikeda E Haneda H Suzuki 2008 Chronic fluoxetine bidirectionally modulates potentiating effects of serotonin on the hippocampal mossy fiber synaptic transmission J Neurosci 28 6272 6280
60. WF Hopkins D Johnston 1988 Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus J Neurophysiol 59 667 687 (Pubitemid 18069331)
61. MG Weisskopf PE Castillo RA Zalutsky RA Nicoll 1994 Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP Science 265 1878 1882 (Pubitemid 24324246)
62. JM O'Donnell H-T Zhang 2004 Antidepressant effects of inhibitors of cAMP phosphodiesterase (PDE4) Trends Pharmacol Sci 25 158 163 (Pubitemid 38264507)
63. CR Maxwell SJ Kanes T Abel SJ Siegel 2004 Phosphodiesterase inhibitors: a novel mechanism for receptor-independent antipsychotic medications Neuroscience 129 101 107 (Pubitemid 39360946)
64. JA Siuciak DS Chapin SA McCarthy AN Martin 2007 Antipsychotic profile of rolipram: efficacy in rats and reduced sensitivity in mice deficient in the phosphodiesterase-4B (PDE4B) enzyme Psychopharmacology (Berl) 192 415 424 (Pubitemid 46701580)
65. E Gould P Tanapat NB Hastings TJ Shors 1999 Neurogenesis in adulthood: a possible role in learning Trends Cogn Sci 3 186 192 (Pubitemid 29215058)
66. H van Praag AF Schinder BR Christie N Toni TD Palmer FH Gage 2002 Functional neurogenesis in the adult hippocampus Nature 415 1030 1034 (Pubitemid 34193451)
67. S Jessberger G Kempermann 2003 Adult-born hippocampal neurons mature into activity-dependent responsiveness Eur J Neurosci 18 2707 2712 (Pubitemid 37542123)
68. N Toni DA Laplagne C Zhao G Lombardi CE Ribak FH Gage AF Schinder 2008 Neurons born in the adult dentate gyrus form functional synapses with target cells Nat Neurosci 11 901 907
69. JE Malberg AJ Eisch EJ Nestler RS Duman 2000 Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus J Neurosci 20 9104 9110 (Pubitemid 32042912)
70. L Santarelli M Saxe C Gross A Surget F Battaglia S Dulawa N Weisstaub J Lee R Duman O Arancio C Belzung R Hen 2003 Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants Science 301 805 809 (Pubitemid 36962615)
71. RD Airan LA Meltzer M Roy Y Gong H Chen K Deisseroth 2007 High-speed imaging reveals neurophysiological links to behavior in an animal model of depression Science 317 819 823 (Pubitemid 47257922)
72. J-W Wang DJ David JE Monckton F Battaglia R Hen 2008 Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells J Neurosci 28 1374 1384 (Pubitemid 351231535)
73. JL Warner-Schmidt RS Duman 2006 Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment Hippocampus 16 239 249
74. A Surget M Saxe S Leman Y Ibarguen-Vargas S Chalon G Griebel R Hen C Belzung 2008 Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal Biol Psychiatry 64 293 301
75. A Reif S Fritzen M Finger A Strobel M Lauer A Schmitt K-P Lesch 2006 Neural stem cell proliferation is decreased in schizophrenia, but not in depression Mol Psychiatry 11 514 522
76. RS Duman LM Monteggia 2006 A neurotrophic model for stress-related mood disorders Biol Psychiatry 59 1116 1127 (Pubitemid 43912554)
77. JM Conner JC Lauterborn Q Yan CM Gall S Varon 1997 Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport J Neurosci 17 2295 2313 (Pubitemid 27137397)
78. MA Smith L-X Zhang WE Lyons LA Mamounas 1997 Anterograde transport of endogenous brain-derived neurotrophic factor in hippocampal mossy fibers Neuroreport 8 1829 1834 (Pubitemid 27314292)
79. M Adachi M Barrot AE Autry D Theobald LM Monteggia 2008 Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy Biol Psychiatry 63 642 649 (Pubitemid 351329281)
80. B Chen D Dowlatshahi GM MacQueen J-F Wang LT Young 2001 Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication Biol Psychiatry 50 260 265 (Pubitemid 32778442)
81. CA Altar RE Whitehead R Chen G Wörtwein TM Madsen 2003 Effects of electroconvulsive seizures and antidepressant drugs on brain-derived neurotrophic factor protein in rat brain Biol Psychiatry 54 703 709 (Pubitemid 37281386)
82. JPR Jacobsen A Mørk 2004 The effect of escitalopram, desipramine, electroconvulsive seizures and lithium on brain-derived neurotrophic factor mRNA and protein expression in the rat brain and the correlation to 5-HT and 5-HIAA levels Brain Res 1024 183 192 (Pubitemid 39286729)
83. DT Balu BA Hoshaw JE Malberg S Rosenzweig-Lipson LE Schechter I Lucki 2008 Differential regulation of central BDNF protein levels by antidepressant and non-antidepressant drug treatments Brain Res 1211 37 43
84. G De Foubert SL Carney CS Robinson EJ Destexhe R Tomlinson CA Hicks TK Murray JP Gaillard C Deville V Xhenseval CE Thomas MJ O'Neill TSC Zetterström 2004 Fluoxetine-induced change in rat brain expression of brain-derived neurotrophic factor varies depending on length of treatment Neuroscience 128 597 604 (Pubitemid 39277429)
85. H Xu JS Richardson X-M Li 2003 Dose-related effects of chronic antidepressants on neuroprotective proteins BDNF, Bcl-2 and Cu/Zn-SOD in rat hippocampus Neuropsychopharmacology 28 53 62
86. R Lee P Kermani KK Teng BL Hempstead 2001 Regulation of cell survival by secreted proneurotrophins Science 294 1945 1948 (Pubitemid 33101595)
87. NTR and sortilin J Neurosci 25 5455 5463 (Pubitemid 40770927)
88. NTR by proBDNF facilitates hippocampal long-term depression Nat Neurosci 8 1069 1077 (Pubitemid 41061518)
89. Z Gombos A Spiller GA Cottrell RJ Racine WM Burnham 1999 Mossy fiber sprouting induced by repeated electroconvulsive shock seizures Brain Res 844 28 33 (Pubitemid 29490949)
90. VA Vaidya JA Siuciak F Du RS Duman 1999 Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures Neuroscience 89 157 166 (Pubitemid 29049035)
91. SR Lamont A Paulls CA Stewart 2001 Repeated electroconvulsive stimulation, but not antidepressant drugs, induces mossy fibre sprouting in the rat hippocampus Brain Res 893 53 58 (Pubitemid 32171896)
92. D Pagnin V de Queiroz S Pini GB Cassano 2004 Efficacy of ECT in depression: a meta-analytic review J ECT 20 13 20 (Pubitemid 38488810)
93. 4 agonists on the population spike recorded in hippocampal CA1 cells do not involve presynaptic effects on excitatory synaptic transmission Pol J Pharmacol 48 565 573
94. 4 receptor activation in the rat hippocampus Naunyn Schmiedebergs Arch Pharmacol 355 14 19 (Pubitemid 27008447)
95. SM Stahl 1998 Mechanism of action of serotonin selective reuptake inhibitors. Serotonin receptors and pathways mediate therapeutic effects and side effects J Affect Disord 51 215 235 (Pubitemid 29202172)
96. M Vaswani FK Linda S Ramesh 2003 Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review Prog Neuropsychopharmacol Biol Psychiatry 27 85 102 (Pubitemid 36131110)
97. S Benmansour M Cecchi DA Morilak GA Gerhardt MA Javors GG Gould A Frazer 1999 Effects of chronic antidepressant treatments on serotonin transporter function, density, and mRNA level J Neurosci 19 10494 10501 (Pubitemid 30228055)
98. S Benmansour WA Owens M Cecchi DA Morilak A Frazer 2002 Serotonin clearance in vivo is altered to a greater extent by antidepressant-induced downregulation of the serotonin transporter than by acute blockade of this transporter J Neurosci 22 6766 6772 (Pubitemid 35386433)
99. BH Miller LE Schultz A Gulati MD Cameron MT Pletcher 2008 Genetic regulation of behavioral and neuronal responses to fluoxetine Neuropsychopharmacology 33 1312 1322
100. I Sillaber M Panhuysen MSH Henniger F Ohl C Kühne B Pütz T Pohl JM Deussing M Paez-Pereda F Holsboer 2008 Profiling of behavioral changes and hippocampal gene expression in mice chronically treated with the SSRI paroxetine Psychopharmacology (Berl) 200 557 572
101. S Ge C-h Yang K-s Hsu G-l Ming H Song 2007 A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain Neuron 54 559 566 (Pubitemid 46756142)
102. CA Stewart IC Reid 2000 Repeated ECS and fluoxetine administration have equivalent effects on hippocampal synaptic plasticity Psychopharmacology (Berl) 148 217 223 (Pubitemid 30136728)
103. JP Chan J Cordeira GA Calderon LK Iyer M Rios 2008 Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus Mol Cell Neurosci 39 372 383
104. HE Scharfman 1997 Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor J Neurophysiol 78 1082 1095 (Pubitemid 27353567)
105. K Kobayashi Y Ikeda A Sakai H Suzuki 2008 Chronic SSRI changes the maturation state of dentate granule cells FENS Abstr 4 181.22
106. DR Weinberger 1999 Cell biology of the hippocampal formation in schizophrenia Biol Psychiatry 45 395 402 (Pubitemid 29130435)
107. PJ Harrison 2004 The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications Psychopharmacology (Berl) 174 151 162 (Pubitemid 38925100)
108. T Bast J Feldon 2003 Hippocampal modulation of sensorimotor processes Prog Neurobiol 70 319 345 (Pubitemid 37107357)
109. EM Joyce JP Roiser 2007 Cognitive heterogeneity in schizophrenia Curr Opin Psychiatry 20 268 272 (Pubitemid 46588300)
110. BI Turetsky ME Calkins GA Light A Olincy AD Radant NR Swerdlow 2007 Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures Schizophr Bull 33 69 94 (Pubitemid 46026260)
111. H Jeltsch F Bertrand C Lazarus J-C Cassel 2001 Cognitive performances and locomotor activity following dentate granule cell damage in rats: role of lesion extent and type of memory tested Neurobiol Learn Mem 76 81 105 (Pubitemid 32566150)
112. V Hernández-Rabaza JA Barcia M Llorens-Martín JL Trejo JJ Canales 2007 Spared place and object-place learning but limited spatial working memory capacity in rats with selective lesions of the dentate gyrus Brain Res Bull 72 315 323 (Pubitemid 46602755)
113. A receptor binding in the hippocampal formation of schizophrenic brain Synapse 22 338 349
114. V Klimek G Rajkowska SN Luker G Dilley HY Meltzer JC Overholser CA Stockmeier GA Ordway 1999 Brain noradrenergic receptors in major depression and schizophrenia Neuropsychopharmacology 21 69 81 (Pubitemid 29253837)
115. R Kerwin S Patel B Meldrum 1990 Quantitative autoradiographic analysis of glutamate binding sites in the hippocampal formation in normal and schizophrenic brain post mortem Neuroscience 39 25 32
116. SL Eastwood B McDonald PWJ Burnet JP Beckwith RW Kerwin PJ Harrison 1995 Decreased expression of mRNAs encoding non-NMDA glutamate receptors GluR1 and GluR2 in medial temporal lobe neurons in schizophrenia Brain Res Mol Brain Res 29 211 223
117. RHP Porter SL Eastwood PJ Harrison 1997 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 751 217 231 (Pubitemid 27132551)
118. X-M Gao K Sakai RC Roberts RR Conley B Dean CA Tamminga 2000 Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia Am J Psychiatry 157 1141 1149 (Pubitemid 30432497)
119. B receptor in the hippocampus of subjects with schizophrenia Neurosci Lett 283 101 104 (Pubitemid 30156743)
120. AJ Law JFW Deakin 2001 Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses Neuroreport 12 2971 2974 (Pubitemid 32882018)
121. R Freedman M Hall LE Adler S Leonard 1995 Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia Biol Psychiatry 38 22 33
122. JM Crook E Tomaskovic-Crook DL Copolov B Dean 2000 Decreased muscarinic receptor binding in subjects with schizophrenia: a study of the human hippocampal formation Biol Psychiatry 48 381 388 (Pubitemid 30687253)
123. SL Eastwood PJ Harrison 1995 Decreased synaptophysin in the medial temporal lobe in schizophrenia demonstrated using immunoautoradiography Neuroscience 69 339 343
124. CE Young K Arima J Xie L Hu TG Beach P Falkai WG Honer 1998 SNAP-25 deficit and hippocampal connectivity in schizophrenia Cereb Cortex 8 261 268 (Pubitemid 28226162)
125. CA Altar LW Jurata V Charles A Lemire P Liu Y Bukhman TA Young J Bullard H Yokoe MJ Webster MB Knable JA Brockman 2005 Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts Biol Psychiatry 58 85 96 (Pubitemid 41008124)
126. NS Kolomeets DD Orlovskaya VI Rachmanova NA Uranova 2005 Ultrastructural alterations in hippocampal mossy fiber synapses in schizophrenia: a postmortem morphometric study Synapse 57 47 55 (Pubitemid 40756334)
127. NS Kolomeets DD Orlovskaya NA Uranova 2007 Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia Synapse 61 615 621 (Pubitemid 46934008)
128. C Nowakowski WA Kaufmann C Adlassnig H Maier K Salimi KA Jellinger J Marksteiner 2002 Reduction of chromogranin B-like immunoreactivity in distinct subregions of the hippocampus from individuals with schizophrenia Schizophr Res 58 43 53 (Pubitemid 35287282)
129. CS Weickert DA Rothmond TM Hyde JE Kleinman RE Straub 2008 Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients Schizophr Res 98 105 110 (Pubitemid 350245587)
130. CMP O'Tuathaigh D Babovic G O'Meara JJ Clifford DT Croke JL Waddington 2007 Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour Neurosci Biobehav Rev 31 60 78 (Pubitemid 44880074)
131. K Takao K Toyama K Nakanishi S Hattori H Takamura M Takeda T Miyakawa R Hashimoto 2008 Impaired long-term memory retention and working memory in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia Mol Brain 1 11
132. T Numakawa Y Yagasaki T Ishimoto T Okada T Suzuki N Iwata N Ozaki T Taguchi M Tatsumi K Kamijima RE Straub DR Weinberger H Kunugi R Hashimoto 2004 Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia Hum Mol Genet 13 2699 2708 (Pubitemid 39485418)
133. X-W Chen Y-Q Feng C-J Hao X-L Guo X He Z-Y Zhou N Guo H-P Huang W Xiong H Zheng P-L Zuo CX Zhang W Li Z Zhou 2008 DTNBP1, a schizophrenia susceptibility gene, affects kinetics of transmitter release J Cell Biol 181 791 801 (Pubitemid 351786984)
134. MA Benson SE Newey E Martin-Rendon R Hawkes DJ Blake 2001 Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain J Biol Chem 276 24232 24241
135. K Talbot WL Eidem CL Tinsley MA Benson EW Thompson RJ Smith C-G Hahn SJ Siegel JQ Trojanowski RE Gur DJ Blake SE Arnold 2004 Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia J Clin Invest 113 1353 1363 (Pubitemid 39069934)
136. SH Fatemi JA Earle T McMenomy 2000 Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression Mol Psychiatry 5 654 663
137. SL Eastwood PJ Harrison 2006 Cellular basis of reduced cortical reelin expression in schizophrenia Am J Psychiatry 163 540 542 (Pubitemid 44469402)
138. L Rioux SE Arnold 2005 The expression of retinoic acid receptor alpha is increased in the granule cells of the dentate gyrus in schizophrenia Psychiatry Res 133 13 21 (Pubitemid 40215467)
139. SE Arnold K Talbot C-G Hahn 2005 Neurodevelopment, neuroplasticity, and new genes for schizophrenia Prog Brain Res 147 319 345
140. D Kamnasaran WJ Muir MA Ferguson-Smith DW Cox 2003 Disruption of the neuronal PAS3 gene in a family affected with schizophrenia J Med Genet 40 325 332 (Pubitemid 36613468)
141. C Erbel-Sieler C Dudley Y Zhou X Wu SJ Estill T Han R Diaz-Arrastia EW Brunskill SS Potter SL McKnight 2004 Behavioral and regulatory abnormalities in mice deficient in the NPAS1 and NPAS3 transcription factors Proc Natl Acad Sci USA 101 13648 13653 (Pubitemid 39238457)
142. AA Pieper X Wu TW Han SJ Estill Q Dang LC Wu S Reece-Fincanon CA Dudley JA Richardson DJ Brat SL McKnight 2005 The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice Proc Natl Acad Sci USA 102 14052 14057 (Pubitemid 41377701)
143. KD Meyer JA Morris 2008 Immunohistochemical analysis of Disc1 expression in the developing and adult hippocampus Gene Expr Patterns 8 494 501
144. CP Austin B Ky L Ma JA Morris PJ Shughrue 2004 Expression of Disrupted-In-Schizophrenia-1, a schizophrenia-associated gene, is prominent in the mouse hippocampus throughout brain development Neuroscience 124 3 10 (Pubitemid 38186612)
145. K Miyoshi A Honda K Baba M Taniguchi K Oono T Fujita S Kuroda T Katayama M Tohyama 2003 Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth Mol Psychiatry 8 685 694 (Pubitemid 36976300)
146. CP Austin L Ma B Ky JA Morris PJ Shughrue 2003 DISC1 (Disrupted in Schizophrenia-1) is expressed in limbic regions of the primate brain Neuroreport 14 951 954 (Pubitemid 36829770)
147. R James RR Adams S Christie SR Buchanan DJ Porteous JK Millar 2004 Disrupted in Schizophrenia 1 (DISC1) is a multicompartmentalized protein that predominantly localizes to mitochondria Mol Cell Neurosci 26 112 122 (Pubitemid 38581027)
148. X Duan JH Chang S Ge RL Faulkner JY Kim Y Kitabatake X-b Liu C-H Yang JD Jordan DK Ma CY Liu S Ganesan H-J Cheng G-l Ming B Lu H Song 2007 Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain Cell 130 1146 1158 (Pubitemid 47422304)
149. M Lauer H Beckmann D Senitz 2003 Increased frequency of dentate granule cells with basal dendrites in the hippocampal formation of schizophrenics Psychiatry Res 122 89 97 (Pubitemid 36506476)
150. RL Faulkner M-H Jang X-B Liu X Duan KA Sailor JY Kim S Ge EG Jones G-l Ming H Song H-J Cheng 2008 Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain Proc Natl Acad Sci USA 105 14157 14162
151. M Kvajo H McKellar PA Arguello LJ Drew H Moore AB MacDermott M Karayiorgou JA Gogos 2008 A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition Proc Natl Acad Sci USA 105 7076 7081 (Pubitemid 351754532)
152. A Contractor G Swanson SF Heinemann 2001 Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus Neuron 29 209 216 (Pubitemid 32108733)
153. 6 at hippocampal mossy fiber synapses J Neurosci 24 10093 10098 (Pubitemid 39492033)
154. G Shaltiel S Maeng O Malkesman B Pearson RJ Schloesser T Tragon M Rogawski M Gasior D Luckenbaugh G Chen HK Manji 2008 Evidence for the involvement of the kainate receptor subunit GluR6 (GRIK2) in mediating behavioral displays related to behavioral symptoms of mania Mol Psychiatry 13 858 872
155. L Seress L Mrzljak 1987 Basal dendrites of granule cells are normal features of the fetal and adult dentate gyrus of both monkey and human hippocampal formations Brain Res 405 169 174 (Pubitemid 17034946)
156. M Blaabjerg J Zimmer 2007 The dentate mossy fibers: structural organization, development and plasticity Prog Brain Res 163 85 107
157. NN Urban DA Henze DA Lewis G Barrionuevo 1996 Properties of LTP induction in the CA3 region of the primate hippocampus Learn Mem 3 86 95 (Pubitemid 26357734)
158. JL St John DL Rosene JI Luebke 1997 Morphology and electrophysiology of dentate granule cells in the rhesus monkey: comparison with the rat J Comp Neurol 387 136 147 (Pubitemid 27419465)
159. OJ Ariwodola TL Crowder KA Grant JB Daunais DP Friedman JL Weiner 2003 Ethanol modulation of excitatory and inhibitory synaptic transmission in rat and monkey dentate granule neurons Alcohol Clin Exp Res 27 1632 1639 (Pubitemid 37280746)
160. O Bai J Chlan-Fourney R Bowen D Keegan X-M Li 2003 Expression of brain-derived neurotrophic factor mRNA in rat hippocampus after treatment with antipsychotic drugs J Neurosci Res 71 127 131 (Pubitemid 36008409)
161. AM Barr CE Young AG Phillips WG Honer 2006 Selective effects of typical antipsychotic drugs on SNAP-25 and synaptophysin in the hippocampal trisynaptic pathway Int J Neuropsychopharmacol 9 457 463 (Pubitemid 43979706)
162. SS Newton RS Duman 2007 Neurogenic actions of atypical antipsychotic drugs and therapeutic implications CNS Drugs 21 715 725 (Pubitemid 47294718)
163. ND Halim CS Weickert BW McClintock DR Weinberger BK Lipska 2004 Effects of chronic haloperidol and clozapine treatment on neurogenesis in the adult rat hippocampus Neuropsychopharmacology 29 1063 1069 (Pubitemid 38670044)
164. M Kodama T Fujioka RS Duman 2004 Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat Biol Psychiatry 56 570 580 (Pubitemid 39336404)
165. A Schmitt S Weber A Jatzko DF Braus FA Henn 2004 Hippocampal volume and cell proliferation after acute and chronic clozapine or haloperidol treatment J Neural Transm 111 91 100 (Pubitemid 38177820)
166. W Green P Patil CA Marsden GW Bennett PM Wigmore 2006 Treatment with olanzapine increases cell proliferation in the subventricular zone and prefrontal cortex Brain Res 1070 242 245 (Pubitemid 43247763)
167. CG Wakade SP Mahadik JL Waller F-c Chiu 2002 Atypical neuroleptics stimulate neurogenesis in adult rat brain J Neurosci Res 69 72 79 (Pubitemid 34734166)
168. H-D Wang FD Dunnavant T Jarman AY Deutch 2004 Effects of antipsychotic drugs on neurogenesis in the forebrain of the adult rat Neuropsychopharmacology 29 1230 1238 (Pubitemid 38780646)
169. TE Kippin S Kapur D van der Kooy 2005 Dopamine specifically inhibits forebrain neural stem cell proliferation, suggesting a novel effect of antipsychotic drugs J Neurosci 25 5815 5823 (Pubitemid 40847894)
170. RR Dawirs K Hildebrandt G Teuchert-Noodt 1998 Adult treatment with haloperidol increases dentate granule cell proliferation in the gerbil hippocampus J Neural Transm 105 317 327 (Pubitemid 28243239)
171. H-J Möller 2003 Management of the negative symptoms of schizophrenia: new treatment options CNS Drugs 17 793 823 (Pubitemid 37082984)
172. PG Strange 2001 Antipsychotic drugs: importance of dopamine receptors for mechanisms of therapeutic actions and side effects Pharmacol Rev 53 119 133 (Pubitemid 32173111)
173. 2 receptor stimulation promotes the proliferation of neural progenitor cells in adult mouse hippocampus Neuroreport 18 659 664 (Pubitemid 46608510)
174. 2 receptor-induced CNS neurogenesis in adult mice J Neurosci 28 2231 2241 (Pubitemid 351317623)
175. N Müller M Schwarz 2006 Schizophrenia as an inflammation-mediated dysbalance of glutamatergic neurotransmission Neurotox Res 10 131 148
176. J Cartmell JA Monn DD Schoepp 1999 The metabotropic glutamate 2/3 receptor agonists LY354740 and LY379268 selectively attenuate phencyclidine versus d-amphetamine motor behaviors in rats J Pharmacol Exp Ther 291 161 170 (Pubitemid 29451586)
177. ST Patil L Zhang F Martenyi SL Lowe KA Jackson BV Andreev AS Avedisova LM Bardenstein IY Gurovich MA Morozova SN Mosolov NG Neznanov AM Reznik AB Smulevich VA Tochilov BG Johnson JA Monn DD Schoepp 2007 Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial Nat Med 13 1102 1107 (Pubitemid 47517511)
178. H Kamiya H Shinozaki C Yamamoto 1996 Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses J Physiol 493 447 455 (Pubitemid 26187504)
179. TA Macek DG Winder RW Gereau IV CO Ladd PJ Conn 1996 Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses J Neurophysiol 76 3798 3806 (Pubitemid 27009683)
180. A Olincy KE Stevens 2007 Treating schizophrenia symptoms with an alpha7 nicotinic agonist, from mice to men Biochem Pharmacol 74 1192 1201 (Pubitemid 47417932)
181. R Freedman A Olincy RW Buchanan JG Harris JM Gold L Johnson D Allensworth A Guzman-Bonilla B Clement MP Ball J Kutnick V Pender LF Martin KE Stevens BD Wagner GO Zerbe F Soti WR Kem 2008 Initial phase 2 trial of a nicotinic agonist in schizophrenia Am J Psychiatry 165 1040 1047
182. S Leonard R Freedman 2006 Genetics of chromosome 15q13-q14 in schizophrenia Biol Psychiatry 60 115 122 (Pubitemid 44026594)
183. 125I]- α-bungarotoxin binding in human postmortem brain J Comp Neurol 387 385 398 (Pubitemid 27430337)
184. JW Young N Crawford JS Kelly LE Kerr HM Marston C Spratt K Finlayson J Sharkey 2007 Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice Eur Neuropsychopharmacol 17 145 155 (Pubitemid 44802833)
185. C Fernandes E Hoyle E Dempster LC Schalkwyk DA Collier 2006 Performance deficit of α7 nicotinic receptor knockout mice in a delayed matching-to-place task suggests a mild impairment of working/episodic-like memory Genes Brain Behav 5 433 440 (Pubitemid 44199563)
186. R Gray AS Rajan KA Radcliffe M Yakehiro JA Dani 1996 Hippocampal synaptic transmission enhanced by low concentrations of nicotine Nature 383 713 716 (Pubitemid 26360646)
187. G Sharma S Vijayaraghavan 2003 Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing Neuron 38 929 939 (Pubitemid 36789765)
188. G Sharma M Grybko S Vijayaraghavan 2008 Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses J Neurosci 28 2563 2575 (Pubitemid 351348186)
189. KE Vogt WG Regehr 2001 Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus J Neurosci 21 75 83 (Pubitemid 32098728)
190. S van Neerven E Kampmann J Mey 2008 RAR/RXR and PPAR/RXR signaling in neurological and psychiatric diseases Prog Neurobiol 85 433 451
191. MJ Webster MB Knable J O'Grady J Orthmann CS Weickert 2002 Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders Mol Psychiatry 7 985 994 (Pubitemid 35333054)
192. WR Perlman E Tomaskovic-Crook DM Montague MJ Webster DR Rubinow JE Kleinman CS Weickert 2005 Alteration in estrogen receptor α mRNA levels in frontal cortex and hippocampus of patients with major mental illness Biol Psychiatry 58 812 824 (Pubitemid 41677420)
193. D Barbeau JJ Liang Y Robitalille R Quirion LK Srivastava 1995 Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains Proc Natl Acad Sci USA 92 2785 2789
194. B Dean K Opeskin G Pavey C Hill N Keks 1997 Changes in protein kinase C and adenylate cyclase in the temporal lobe from subjects with schizophrenia J Neural Transm 104 1371 1381 (Pubitemid 28031831)
195. SY Tian J-F Wang YB Bezchlibnyk LT Young 2007 Immunoreactivity of 43 kDa growth-associated protein is decreased in post mortem hippocampus of bipolar disorder and schizophrenia Neurosci Lett 411 123 127 (Pubitemid 44820684)
196. SK Goldsmith JN Joyce 1995 Alterations in hippocampal mossy fiber pathway in schizophrenia and Alzheimer's disease Biol Psychiatry 37 122 126