ENU-mutagenesis mice with a non-synonymous mutation in Grin1 exhibit abnormal anxiety-like behaviors, impaired fear memory, and decreased acoustic startle response

BMC Research Notes

Volumn 6, Issue 1, 2013, Pages

  Umemori, Juzoh ^a,b   Takao, Keizo ^b,c,d   Koshimizu, Hisatsugu ^a,b   Hattori, Satoko ^a,b   Furuse, Tamio ^e   Wakana, Shigeharu ^e   Miyakawa, Tsuyoshi ^a,b,c,d  

^a FUJITA HEALTH UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e RIKEN BIORESOURCE CENTER   (Japan)

Author keywords

ADHD; Comprehensive behavioral test battery; ENU mutagenesis; Grin1; NMDA receptor; Psychiatric disorder; Schizophrenia

Indexed keywords

ANIMALIA; MUS;

CARRIER PROTEIN; ETHYLNITROSOUREA; GPRIN1 PROTEIN, MOUSE; NERVE PROTEIN;

ACOUSTICS; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; ARTICLE; FEAR; GENETICS; LOCOMOTION; MEMORY; MOUSE; MOUSE MUTANT; MUTAGENESIS; STARTLE REFLEX;

ACOUSTICS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CARRIER PROTEINS; ETHYLNITROSOUREA; FEAR; LOCOMOTION; MEMORY; MICE; MICE, MUTANT STRAINS; MUTAGENESIS; NERVE TISSUE PROTEINS; STARTLE REACTION;

EID: 84877888175     PISSN: None     EISSN: 17560500     Source Type: Journal    
DOI: 10.1186/1756-0500-6-203     Document Type: Article

References (89)

1. NMDA receptor subunits: diversity, development and disease. Cull-Candy S, Brickley S, Farrant M, Curr Opin Neurobiol 2001 11 327 335 10.1016/S0959- 4388(00)00215-4 11399431 (Pubitemid 32524098)
2. Molecular characterization of NMDA and metabotropic glutamate receptors. Masu M, Nakajima Y, Moriyoshi K, Ishii T, Akazawa C, Nakanashi S, Ann N Y Acad Sci 1993 707 153 164 10.1111/j.1749-6632.1993.tb38050.x 9137550 (Pubitemid 24099475)
3. NMDA receptors: from genes to channels. Sucher NJ, Awobuluyi M, Choi Y-B, Lipton SA, Trends Pharmacol Sci 1996 17 348 355 8979769 (Pubitemid 26377116)
4. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Tsien JZ, Huerta PT, Tonegawa S, Cell 1996 87 1327 1338 10.1016/S0092-8674(00)81827-9 8980238 (Pubitemid 27010115)
5. Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D- aspartate receptor antagonist AP5. Morris RG, J Neurosci 1989 9 3040 3057 2552039 (Pubitemid 19260822)
6. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY, Nature 1994 368 144 147 Published online: 10 March 1994 10.1038/368144a0 8139656 (Pubitemid 24101524)
7. A synaptic model of memory: long-term potentiation in the hippocampus. Bliss TVP, Collingridge GL, Nature 1993 361 31 39 Published online: 07 January 1993 10.1038/361031a0 8421494 (Pubitemid 23020772)
8. The glutamate receptor ion channels. Dingledine R, Borges K, Bowie D, Traynelis SF, Pharmacol Rev 1999 51 7 62 10049997
9. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH, Neuron 1994 12 529 540 10.1016/0896-6273(94)90210-0 7512349 (Pubitemid 24100885)
10. The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Goff DC, Am J Psychiatry 2001 158 1367 1377 10.1176/appi.ajp.158. 9.1367 11532718 (Pubitemid 32847232)
11. Glutamate and schizophrenia: beyond the dopamine hypothesis. Coyle J, Cell Mol Neurobiol 2006 26 363 382 10.1007/s10571-006-9062-8
12. N-methyl-D-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia? Kantrowitz JT, Javitt DC, Brain Res Bull 2010 83 108 121 10.1016/j.brainresbull.2010.04.006 20417696
13. Glutamatergic theories of schizophrenia. Javitt DC, Isr J Psychiatry Relat Sci 2010 47 4 16 20686195
14. NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A, Neuropsychopharmacology 1996 14 301 307 10.1016/0893-133X(95)00137-3 8703299 (Pubitemid 26151927)
15. Significant association between the genetic variations in the 5′ end of the N-Methyl-D-Aspartate receptor subunit gene GRIN1 and schizophrenia. Zhao X, Li H, Shi Y, Tang R, Chen W, Liu J, Feng G, Shi J, Yan L, Liu H, He L, Biol Psychiatry 2006 59 747 753 10.1016/j.biopsych.2005.10.023 16476413
16. Possible association between genetic variants at the GRIN1 gene and schizophrenia with lifetime history of depressive symptoms in a German sample. Georgi A, Jamra RA, Klein K, Villela AW, Schumacher J, Becker T, Paul T, Schmael C, Höfels S, Klopp N, Illig T, Propping P, Cichon S, Nöthen MM, Schulze TG, Rietschel M, Psychiatr Genet 2007 17 308 310 10.1097/YPG. 0b013e3280c1e5fb 17728671 (Pubitemid 47345754)
17. Association between the G1001C polymorphism in the GRIN1 gene promoter and schizophrenia in the Iranian population. Galehdari H, J Mol Neurosci 2009 38 178 181 10.1007/s12031-008-9148-5 18792810
18. Association of GRIN1 and GRIN2A-D With schizophrenia and genetic interaction with maternal herpes simplex virus-2 infection affecting disease risk. Demontis D, Nyegaard M, Buttenschøn HN, Hedemand A, Pedersen CB, Grove J, Flint TJ, Nordentoft M, Werge T, Hougaard DM, Sørensen KM, Yolken RH, Mors O, Børglum AD, Mortensen PB, Am J Med Genet B 2011 156 913 922 10.1002/ajmg.b.31234
19. Identification of single-nucleotide polymorphisms in the human N-methyl-D-aspartate receptor subunit NR2D gene, GRIN2D, and association study with schizophrenia. Makino C, Shibata H, Ninomiya H, Tashiro N, Fukumaki Y, Psychiatr Genet 2005 15 215 221 10.1097/00041444-200509000-00014 16094258 (Pubitemid 41231946)
20. Evidence that the N-methyl-D-aspartate subunit 1 receptor gene (GRIN1) confers susceptibility to bipolar disorder. Mundo E, Tharmalingham S, Neves-Pereira M, Dalton EJ, Macciardi F, Parikh SV, Bolonna A, Kerwin RW, Arranz MJ, Makoff AJ, Kennedy JL, Mol Psychiatr 2003 8 241 245 10.1038/sj.mp.4001218 (Pubitemid 36315234)
21. Association of the glutamate receptor subunit gene GRIN2B with attentiondeficit/hyperactivity disorder, Association of the glutamate receptor subunit gene GRIN2B with attentiondeficit/hyperactivity disorder. Dorval KM, Wigg KG, Crosbie J, Tannock R, Kennedy JL, Ickowicz A, Pathare T, Malone M, Schachar R, Barr CL, Dorval KM, Wigg KG, Crosbie J, Tannock R, Kennedy JL, Ickowicz A, Pathare T, Malone M, Schachar R, Barr CL, Gene Brain Behav 2007 6 444 452 10.1111/j.1601-183X.2006.00273.x (Pubitemid 47024958)
22. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Mohn AR, Gainetdinov RR, Caron MG, Koller BH, Cell 1999 98 427 436 10.1016/S0092-8674(00)81972-8 10481908 (Pubitemid 29402481)
23. Assessment of NMDA receptor NR1 subunit hypofunction in mice as a model for schizophrenia. Halene TB, Ehrlichman RS, Liang Y, Christian EP, Jonak GJ, Gur TL, Blendy JA, Dow HC, Brodkin ES, Schneider F, Gur RC, Siegel SJ, Genes Brain Behav 2009 8 661 675 10.1111/j.1601-183X.2009.00504.x 19563516
24. Deficits in sensorimotor gating and tests of social behavior in a genetic model of reduced NMDA receptor function. Duncan GE, Moy SS, Perez A, Eddy DM, Zinzow WM, Lieberman JA, Snouwaert JN, Koller BH, Behav Brain Res 2004 153 507 519 10.1016/j.bbr.2004.01.008 15265649 (Pubitemid 38953128)
25. Schizophrenia-relevant behavioral testing in rodent models: a uniquely human disorder? Powell CM, Miyakawa T, Biol Psychiatr 2006 59 1198 1207 10.1016/j.biopsych.2006.05.008
26. Severe impairment of NMDA receptor function in mice carrying targeted point mutations in the glycine binding site results in drug-resistant nonhabituating hyperactivity. Ballard TM, Pauly-Evers M, Higgins GA, Ouagazzal A-M, Mutel V, Borroni E, Kemp JA, Bluethmann H, Kew JNC, J Neurosci 2002 22 6713 6723 12151550 (Pubitemid 35386427)
27. Mutant mice with reduced NMDA-NR1 glycine affinity or lack of d-amino acid oxidase function exhibit altered anxiety-like behaviors. Labrie V, Clapcote SJ, Roder JC, Pharmacol Biochem Behav 2009 91 610 620 10.1016/j.pbb.2008.09.016 18940194
28. Selective effects of methylphenidate in attention deficit hyperactivity disorder: A functional magnetic resonance study. Vaidya CJ, Austin G, Kirkorian G, Ridlehuber HW, Desmond JE, Glover GH, Gabrieli JDE, PNAS 1998 95 14494 14499 10.1073/pnas.95.24.14494 9826728 (Pubitemid 28549395)
29. NMDA receptor phosphorylation at a site affected in schizophrenia controls synaptic and behavioral plasticity. Li B, Devidze N, Barengolts D, Prostak N, Sphicas E, Apicella AJ, Malinow R, Emamian ES, J Neurosci 2009 29 11965 11972 10.1523/JNEUROSCI.2109-09.2009 19776282
30. Genetic loss of D-amino acid oxidase activity reverses schizophrenia-like phenotypes in mice. Labrie V, Wang W, Barger SW, Baker GB, Roder JC, Genes Brain Behav 2010 9 11 25 10.1111/j.1601-183X.2009.00529.x 19751394
31. Functional consequences of reduction in NMDA receptor glycine affinity in mice carrying targeted point mutations in the glycine binding site. Kew JNC, Koester A, Moreau J-L, Jenck F, Ouagazzal A-M, Mutel V, Richards JG, Trube G, Fischer G, Montkowski A, Hundt W, Reinscheid RK, Pauly-Evers M, Kemp JA, Bluethmann H, J Neurosci 2000 20 4037 4049 10818139 (Pubitemid 30365674)
32. Phenotypic characterization of a new Grin1 mutant mouse generated by ENU mutagenesis. Furuse T, Wada Y, Hattori K, Yamada I, Kushida T, Shibukawa Y, Masuya H, Kaneda H, Miura I, Seno N, Kanda T, Hirose R, Toki S, Nakanishi K, Kobayashi K, Sezutsu H, Gondo Y, Noda T, Yuasa S, Wakana S, Eur J Neurosci 2010 31 1281 1291 10.1111/j.1460-9568.2010.07164.x 20345915
33. Dopamine dysfunction in AD/HD: integrating clinical and basic neuroscience research. Solanto MV, Behav Brain Res 2002 130 65 71 10.1016/S0166-4328(01)00431-4 11864719 (Pubitemid 34195322)
34. Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Castellanos FX, Tannock R, Nat Rev Neurosci 2002 3 617 628 12154363 (Pubitemid 135706670)
35. Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Yamasaki N, Maekawa M, Kobayashi K, Kajii Y, Maeda J, Soma M, Takao K, Tanda K, Ohira K, Toyama K, Kanzaki K, Fukunaga K, Sudo Y, Ichinose H, Ikeda M, Iwata N, Ozaki N, Suzuki H, Higuchi M, Suhara T, Yuasa S, Miyakawa T, Mol Brain 2008 1 6 10.1186/1756-6606-1-6 18803808
36. Immature dentate gyrus: An endophenotype of neuropsychiatric disorders. Hagihara H, Takao K, Walton N, Matsumoto M, Miyakawa T, Neural Plasticity in press
37. Synaptosomal-associated protein 25 mutation induces immaturity of the dentate granule cells of adult mice. Ohira K, Kobayashi K, Toyama K, Nakamura HK, Shoji H, Takao K, Takeuchi R, Yamaguchi S, Kataoka M, Otsuka S, Takahashi M, Miyakawa T, Mol Brain 2013 6 12 10.1186/1756-6606-6-12 23497716
38. Deficiency of Schnurri-2, an MHC Enhancer Binding Protein, Induces Mild Chronic Inflammation in the Brain and Confers Molecular, Neuronal, and Behavioral Phenotypes Related to Schizophrenia. Takao K, Kobayashi K, Hagihara H, Ohira K, Shoji H, Hattori S, Koshimizu H, Umemori J, Toyama K, Nakamura HK, Kuroiwa M, Maeda J, Atsuzawa K, Esaki K, Yamaguchi S, Furuya S, Takagi T, Walton NM, Hayashi N, Suzuki H, Higuchi M, Usuda N, Suhara T, Nishi A, Matsumoto M, Ishii S, Miyakawa T, Neuropsychopharmacology 2013 Epub ahead of print 10.1038/npp.2013.38
39. Comprehensive behavioral analysis of pituitary adenylate cyclase-activating polypeptide (PACAP) knockout mice. Hattori S, Takao K, Tanda K, Toyama K, Shintani N, Hashimoto H, Miyakawa T, Front Behav Neurosci 2012 6 58 23060763
40. Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Walton NM, Zhou Y, Kogan JH, Shin R, Webster M, Gross AK, Heusner CL, Chen Q, Miyake S, Tajinda K, Tamura K, Miyakawa T, Matsumoto M, Translational Psychiatry 2012 2 135 10.1038/tp.2012.56 22781168
41. Regulation of calcium/calmodulin-dependent protein Kinase II docking toN-Methyl-d-aspartate receptors by calcium/calmodulin and α-actinin. Leonard AS, Bayer K-U, Merrill MA, Lim IA, Shea MA, Schulman H, Hell JW, J Biol Chem 2002 277 48441 48448 10.1074/jbc.M205164200 12379661 (Pubitemid 35470802)
42. Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Holmes A, Yang RJ, Murphy DL, Crawley JN, Neuropsychopharmacology 2001 27 914 923 (Pubitemid 35447628)
43. Differences among eight inbred strains of mice in motor ability and motor learning on a rotorod. McFadyen MP, Kusek G, Bolivar VJ, Flaherty L, Genes Brain Behav 2003 2 214 219 10.1034/j.1601-183X.2003.00028.x 12953787 (Pubitemid 37010665)
44. A method for assessing balance control in rodents. Mulligan SJ, Knapp E, Thompson B, Jung R, Biomed Sci Instrum 2002 38 77 82 12085661 (Pubitemid 35005946)
45. The emotional brain, fear, and the amygdala. LeDoux J, Cell Mol Neurobiol 2003 23 727 738 10.1023/A:1025048802629 14514027 (Pubitemid 37071496)
46. Are fear memories made and maintained by the same NMDA receptor-dependent mechanisms? Walker DL, Davis M, Neuron 2004 41 680 682 10.1016/S0896-6273(04) 00114-X 15003167 (Pubitemid 38326830)
47. Neuronal signalling of fear memory. Maren S, Quirk GJ, Nat Rev Neurosci 2004 5 844 852 10.1038/nrn1535 15496862 (Pubitemid 39482153)
48. Injections of the NMDA receptor antagonist aminophosphonopentanoic acid into the lateral nucleus of the amygdala block the expression of fear-potentiated startle and freezing. Fendt M, J Neurosci 2001 21 4111 4115 11356899 (Pubitemid 32466503)
49. N-methyl-D-aspartate receptor antagonist APV blocks acquisition but not expression of fear conditioning. Kim JJ, DeCola JP, Landeira-Fernandez J, Fanselow MS, Behav Neurosci 1991 105 126 133 1673846
50. Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Gewirtz JC, Davis M, Nature 1997 388 471 474 10.1038/41325 9242405 (Pubitemid 27328924)
51. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Shimizu E, Tang YP, Rampon C, Tsien JZ, Science 2000 290 1170 1174 10.1126/science.290.5494.1170 11073458
52. Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Cui Z, Wang H, Tan Y, Zaia KA, Zhang S, Tsien JZ, Neuron 2004 41 781 793 10.1016/S0896-6273(04)00072-8 15003177 (Pubitemid 38326840)
53. The mouse light/dark box test. Bourin M, Hascoët M, Eur J Pharmacol 2003 463 55 65 10.1016/S0014-2999(03)01274-3 12600702 (Pubitemid 36205072)
54. Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Miyakawa T, Leiter LM, Gerber DJ, Gainetdinov RR, Sotnikova TD, Zeng H, Caron MG, Tonegawa S, Proc Natl Acad Sci 2003 100 8987 8992 10.1073/pnas.1432926100 12851457 (Pubitemid 36899210)
55. Behavioral profile of wild mice in the elevated plus-maze test for anxiety. Holmes A, Parmigiani S, Ferrari P, Palanza P, Rodgers R, Physiol Behav 2000 71 509 516 10.1016/S0031-9384(00)00373-5 11239669 (Pubitemid 32184775)
56. Comprehensive behavioral analysis of pituitary adenylate cyclase-activating polypeptide (PACAP) knockout mice. Keizo T, Tanda K, Toyama K, Shintani N, Hashimoto H, Miyakawa T, Front Behav Neurosci 2012 6 58 23060763
57. Brain corticosteroid receptor balance in health and disease. De Kloet ER, Vreugdenhil E, Oitzl MS, Joëls M, Endocr Rev 1998 19 269 301 10.1210/er.19.3.269 9626555 (Pubitemid 29117816)
58. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE, Front Neuroendocrinol 2003 24 151 180 10.1016/j.yfrne.2003.07.001 14596810 (Pubitemid 37336539)
59. Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze. Silveira MCL, Sandner G, Graeff FG, Behav Brain Res 1993 56 115 118 10.1016/0166-4328(93)90028-O 8397853 (Pubitemid 23272750)
60. Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety. Duncan GE, Knapp DJ, Breese GR, Brain Res 1996 713 79 91 10.1016/0006-8993(95)01486-1 8724978 (Pubitemid 26114832)
61. Responses of Swiss-Webster mice to repeated plus-maze experience: further evidence for a qualitative shift in emotional state? Holmes A, Rodgers RJ, Pharmacol Biochem Behav 1998 60 473 488 10.1016/S0091-3057(98)00008-2 9632231 (Pubitemid 28282689)
62. The use of behavioral test batteries: effects of training history. McIlwain KL, Merriweather MY, Yuva-Paylor LA, Paylor R, Physiol Behav 2001 73 705 717 10.1016/S0031-9384(01)00528-5 11566205 (Pubitemid 32885560)
63. Ethanol-related behaviors in mice lacking the NMDA receptor NR2A subunit. Boyce-Rustay JM, Holmes A, Psychopharmacology 2006 187 455 466 10.1007/s00213-006-0448-6 16835771 (Pubitemid 44200517)
64. Dysfunctions in mice by NMDA receptor point mutations NR1(N598Q) and NR1(N598R). Single FN, Rozov A, Burnashev N, Zimmermann F, Hanley DF, Forrest D, Curran T, Jensen V, Hvalby Ø Sprengel R, Seeburg PH, J Neurosci 2000 20 2558 2566 10729336 (Pubitemid 30220343)
65. Absence of Whisker-related pattern formation in mice with NMDA receptors lacking coincidence detection properties and calcium signaling. Rudhard Y, Kneussel M, Nassar MA, Rast GF, Annala AJ, Chen PE, Tigaret CM, Dean I, Roes J, Gibb AJ, Hunt SP, Schoepfer R, J Neurosci 2003 23 2323 2332 12657691 (Pubitemid 36368920)
66. An association study of the N-methyl-D-aspartate receptor NR1 subunit gene (GRIN1) and NR2B subunit gene (GRIN2B) in schizophrenia with universal DNA microarray. Qin S, Zhao X, Pan Y, Liu J, Feng G, Fu J, Bao J, Zhang Z, He L, Eur J Hum Genet 2005 13 807 814 10.1038/sj.ejhg.5201418 15841096 (Pubitemid 40946078)
67. Glutamatergic mechanisms in schizophrenia. Tsai G, Coyle JT, Annu Rev Pharmacol Toxicol 2002 42 165 179 10.1146/annurev.pharmtox.42.082701.160735 11807169 (Pubitemid 34160524)
68. Working memory dysfunction in schizophrenia. Goldman-Rakic PS, J Neuropsychiatry Clin Neurosci 1994 6 348 357 7841806 (Pubitemid 24344855)
69. Cognitive impairment in schizophrenia is the core of the disorder. Elvevåg B, Goldberg TE, Crit Rev Neurobiol 2000 14 1 21 11253953 (Pubitemid 32193047)
70. Relationship between panic and schizophrenia. Hofmann SG, Depress Anxiety 1999 9 101 106 10.1002/(SICI)1520-6394(1999)9:3<101::AID-DA1>3.0.CO;2-1 10356647 (Pubitemid 29239572)
71. Anxiety and the schizophrenic process: clinical and epidemiological evidence. Turnbull G, Bebbington P, Soc Psychiatry Psychiatr Epidemiol 2001 36 235 243 10.1007/s001270170054 11515701 (Pubitemid 32694468)
72. The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Andrieux A, Salin PA, Vernet M, Kujala P, Baratier J, Gory-Fauré S, Bosc C, Pointu H, Proietto D, Schweitzer A, Denarier E, Klumperman J, Job D, Genes Dev 2002 16 2350 2364 10.1101/gad.223302 12231625 (Pubitemid 35034405)
73. The role of the amygdala in fear and anxiety. Davis M, Annu Rev Neurosci 1992 15 353 375 10.1146/annurev.ne.15.030192.002033 1575447
74. Fear-potentiated startle in two strains of inbred mice. Falls WA, Carlson S, Turner JG, Willott JF, Behav Neurosci 1997 111 855 861 9267664 (Pubitemid 27335398)
75. Handbook of clinical audiology (5th Ed.) KATZ Jack: Librairie Lavoisier http://www.lavoisier.fr/livre/notice.asp?ouvrage=1489029
76. Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Zheng QY, Johnson KR, Erway LC, Hear Res 1999 130 94 107 10.1016/S0378-5955(99)00003-9 10320101 (Pubitemid 29172586)
77. Sensorimotor gating in boys with Tourette's syndrome and ADHD: Preliminary results. Castellanos FX, Fine EJ, Kaysen D, Marsh WL, Rapoport JL, Hallett M, Biol Psychiatry 1996 39 33 41 10.1016/0006-3223(95)00101-8 8719124 (Pubitemid 26022681)
78. Schizophrenia. Van Os J, Kapur S, Lancet 2009 374 635 645 10.1016/S0140-6736(09)60995-8 19700006
79. Monoamine transporters: from genes to behavior. Gainetdinov RR, Caron MG, Annu Rev Pharmacol Toxicol 2003 43 261 284 10.1146/annurev.pharmtox.43.050802. 112309 12359863 (Pubitemid 37372642)
80. Light/dark transition test for mice. Takao K, Miyakawa T, J Vis Exp 2006 1 104 18704188
81. Elevated plus maze for mice. Komada M, Takao K, Miyakawa T, J Vis Exp 2008 22 1088
82. Abnormal social behavior, hyperactivity, impaired remote spatial memory, and increased D1-mediated dopaminergic signaling in neuronal nitric oxide synthase knockout mice. Tanda K, Nishi A, Matsuo N, Nakanishi K, Yamasaki N, Sugimoto T, Toyama K, Takao K, Miyakawa T, Mol Brain 2009 2 19 10.1186/1756-6606-2-19 19538708
83. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, Piven J, Crawley JN, Genes Brain Behav 2004 3 287 302 10.1111/j.1601-1848.2004.00076.x 15344922 (Pubitemid 39277416)
84. Hyperactivity and Intact Hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. Miyakawa T, Yamada M, Duttaroy A, Wess J, J Neurosci 2001 21 5239 5250 11438599 (Pubitemid 32622949)
85. Spatial memory and hippocampal function. Olton DS, Papas BC, Neuropsychologia 1979 17 669 682 10.1016/0028-3932(79)90042-3 522981 (Pubitemid 10167907)
86. Van der Staay FJ, The study of behavioral dysfunctions: an evaluation of selected animal models University of Groningen 2000 http://bibliotheek.eldoc.ub. rug.nl/root/UB/2000/f.j.van.der.staay/
87. A PCR primer bank for quantitative gene expression analysis. Wang X, Seed B, Nucl Acids Res 2003 31 154 e154 10.1093/nar/gng154 14654707
88. A comprehensive collection of experimentally validated primers for Polymerase Chain Reaction quantitation of murine transcript abundance. Spandidos A, Wang X, Wang H, Dragnev S, Thurber T, Seed B, BMC Genomics 2008 9 633 10.1186/1471-2164-9-633 19108745
89. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Spandidos A, Wang X, Wang H, Seed B, Nucleic Acids Res 2009 38 792 D799 19906719