Mouse Models of Hereditary Mental Retardation

Contemporary Clinical Neuroscience

Volumn , Issue , 2006, Pages 101-125

  Welzl, Hans ^a   D’Adamo, Patrizia ^a   Wolfer, David P ^a   Lipp, Hans Peter ^a  

^a NONE

Author keywords

genetic disorders; Mental retardation; mouse models; X linked MR

Indexed keywords

EID: 70349803541     PISSN: 2627535X     EISSN: 26275341     Source Type: Book Series    
DOI: 10.1007/978-1-59745-058-4_6     Document Type: Chapter

References (127)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. Washington, DC: American Psychiatric Association, 1994.
2. World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders: Diagnostic Criteria for Research. Geneva: World Health Organization, 2003.
3. Luckasson R, Borthwick-Duffy S, eds. AAMR—Mental Retardation Definition, Classification, and Systems of Support. Washington, DC: American Association on Mental Retardation, 2002.
4. McLaren J, Bryson SE. Review of recent epidemiological studies of mental retardation: prevalence, associated disorders, and etiology. Am J Ment Retard 1987;92:243–254.
5. Menkes JH, Migeon BR. Biochemical and genetic aspects of mental retardation. Annu Rev Med 1966;17:407–430.
6. Neri G, Opitz JM. Sixty years of X-linked mental retardation: a historical footnote. Am J Med Genet 2000;97:228–233.
7. Lejeune J, Gautier M, Turpin R. Les chromosomes somatique des enfants mongoliens. C R Hebd Seances Acad Sci 1959;248:1721–1722.
8. Kremer EJ, Pritchard M, Lynch M, et al. Mapping of DNA instability at the fragile X to a trinucleotide repeat sequence p(CCG)n. Science 1991;252:1711–1714.
9. Verkerk AJ, Pieretti M, Sutcliffe JS, et al. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 1991;65:905–914.
10. Scriver CR, Eisensmith RC, Woo SLC, Kaufman S. The hyperphenylalaninemias of man and mouse. Annu Rev Genet 1994;28:141–166.
11. Pruitt KD, Maglott DR. RefSeq and LocusLink: NCBI gene-centered resources. Nucleic Acids Res 2001;29:137–140.
12. Plomin R. The genetics of g in human and mouse. Nat Rev Neurosci 2001;2:136–141.
13. Toniolo D, D’Adamo P. X-linked non-specific mental retardation. Curr Opin Genet Dev 2000;10:280–285.
14. O’Donnell WT, Warren ST. A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci 2002;25:315–338.
15. Turner G, Webb T, Wake S, Robinson H. Prevalence of fragile X syndrome. Am J Med Genet 1996;64:196–197.
16. Bakker CE, de Diego Otero Y, Bontekoe C, et al. Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse. Exp Cell Res 2000;258:162–170.
17. Ashley CT, Sutcliffe JS, Kunst CB, et al. Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG-repeat. Nat Genet 1993;4:244–251.
18. Hergersberg M, Matsuo K, Gassmann M, et al. Tissue-specific expression of a FMR1/beta-galactosidase fusion gene in transgenic mice. Hum Mol Genet 1995;4:359–366.
19. Bontekoe CJ, Bakker CE, Nieuwenhuizen IM, et al. Instability of a (CGG)98 repeat in the Fmr1 promoter. Hum Mol Genet 2001;10:1693–1699.
20. Bakker CE, Verheij C, Willemsen R, et al. Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell 1994;78:23–33.
21. Kooy RF, D’Hooge R, Reyniers E, et al. Transgenic mouse model for the fragile X syndrome. Am J Med Genet 1996;64:241–245.
22. Slegtenhorst-Eegdeman KE, de Rooij DG, Verhoef-Post M, et al. Macroorchidism in FMR1 knockout mice is caused by increased Sertoli cell proliferation during testicular development. Endocrinology 1998;139:156–162.
23. Beckel-Mitchener A, Greenough WT. Correlates across the structural, functional, and molecular phenotypes of fragile X syndrome. Ment Retard Dev Disabil Res Rev 2004;10:53–59.
24. Weiler IJ, Spangler CC, Klintsova AY, et al. Fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses. Proc Natl Acad Sci USA 2004;101:17,504–17,509.
25. Steward O, Bakker CE, Willems PJ, Oostra BA. No evidence for disruption of normal patterns of mRNA localization in dendrites or dendritic transport of recently synthesized mRNA in FMR1 knockout mice, a model for human fragile-X mental retardation syndrome. Neuroreport 1998;9:477–481.
26. Ivanco TL, Greenough WT. Altered mossy fiber distributions in adult Fmr1 (FVB) knockout mice. Hippocampus 2002;12:47–54.
27. Mineur YS, Sluyter F, de Wit S, Oostra BA, Crusio WE. Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus 2002;12:39–46.
28. Godfraind JM, Reyniers E, De Boulle K, et al. Long-term potentiation in the hippocampus of fragile X knockout mice. Am J Med Genet 1996;64:246–251.
29. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, Warren ST. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 1999;94:185–192.
30. Li J, Pelletier MR, Perez Velazquez JL, Carlen PL. Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Mol Cell Neurosci 2002;19:138–151.
31. Huber KM, Gallagher SM, Warren ST, Bear MF. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 2002;99:7746–7750.
32. Chen RZ, Akbarian S, Tudor M, Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 2001;27:327–331.
33. Incorpora G, Sorge G, Sorge A, Pavone L. Epilepsy in fragile X syndrome. Brain Dev 2002;24:766–769.
34. Nielsen DM, Derber WJ, McClellan DA, Crnic LS. Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res 2002;927:8–17.
35. Chen L, Toth M. Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 2001;103:1043–1050.
36. Frankland PW, Wang Y, Rosner B, et al. Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice. Mol Psychiatry 2004;9:417–425.
37. Musumeci SA, Bosco P, Calabrese G, et al. Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 2000;41:19–23.
38. Todd PK, Mack KJ. Sensory stimulation increases cortical expression of the fragile X mental retardation protein in vivo. Brain Res Mol Brain Res 2000;80:17–25.
39. Peier AM, McIlwain KL, Kenneson A, Warren ST, Paylor R, Nelson DL. (Over)correction of FMR1 deficiency with YAC transgenics: behavioral and physical features. Hum Mol Genet 2000;9:1145–1159.
40. Qin M, Kang J, Smith CB. Increased rates of cerebral glucose metabolism in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 2002;99:15,758–15,763.
41. Dobkin C, Rabe A, Dumas R, El Idrissi A, Haubenstock H, Brown WT. Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 2000;100:423–429.
42. Van Dam D, D’Hooge R, Hauben E, et al. Spatial learning, contextual fear conditioning and conditioned emotional response in Fmr1 knockout mice. Behav Brain Res 2000;117:127–136.
43. D’Hooge R, Nagels G, Franck F, et al. Mildly impaired water maze performance in male Fmr1 knockout mice. Neuroscience 1997;76:367–376.
44. Fisch GS, Hao HK, Bakker C, Oostra BA. Learning and memory in the FMR1 knockout mouse. Am J Med Genet 1999;84:277–282.
45. Mientjes EJ, Willemsen R, Kirkpatrick LL, et al. Fxr1 knockout mice show a striated muscle phenotype: implications for Fxr1p function in vivo. Hum Mol Genet 2004;13:1291–1302.
46. Bontekoe CJ, McIlwain KL, Nieuwenhuizen IM, et al. Knockout mouse model for Fxr2: a model for mental retardation. Hum Mol Genet 2002;11:487–498.
47. Knight SJ, Flannery AV, Hirst MC, et al. Trinucleotide repeat amplification and hypermethylation of a CpG island in FRAXE mental retardation. Cell 1993;74:127–134.
48. Gu Y, Nelson DL. FMR2 function: insight from a mouse knockout model. Cytogenet Genome Res 2003;100:129–139.
49. Gecz J. The FMR2 gene, FRAXE and non-specific X-linked mental retardation: clinical and molecular aspects. Ann Hum Genet 2000;64:95–106.
50. Hillman MA, Gecz J. Fragile XE-associated familial mental retardation protein 2 (FMR2) acts as a potent transcription activator. J Hum Genet 2001;46:251–259.
51. Chakrabarti L, Bristulf J, Foss GS, Davies KE. Expression of the murine homologue of FMR2 in mouse brain and during development. Hum Mol Genet 1998;7:441–448.
52. Gu Y, McIlwain KL, Weeber EJ, et al. Impaired conditioned fear and enhanced long-term potentiation in Fmr2 knock-out mice. J Neurosci 2002;22:2753–2763.
53. Hanauer A, Young ID. Coffin-Lowry syndrome: clinical and molecular features. J Med Genet 2002;39:705–713.
54. Jacquot S, Zeniou M, Touraine R, Hanauer A. X-linked Coffin-Lowry syndrome (CLS, MIM 303600, RPS6KA3 gene, protein product known under various names: pp90(rsk2), RSK2, ISPK, MAPKAP1). Eur J Hum Genet 2002;10:2–5.
55. Trivier E, De Cesare D, Jacquot S, et al. Mutations in the kinase Rsk-2 associated with Coffin Lowry syndrome. Nature 1996;384:567–570.
56. Delaunoy J, Abidi F, Zeniou M, et al. Mutations in the X-linked RSK2 gene (RPS6KA3) in patients with Coffin-Lowry syndrome. Hum Mutat 2001;17:103–116.
57. Zeniou M, Ding T, Trivier E, Hanauer A. Expression analysis of RSK gene family members: the RSK2 gene, mutated in Coffin-Lowry syndrome, is prominently expressed in brain structures essential for cognitive function and learning. Hum Mol Genet 2002;11:2929–2940.
58. Dufresne SD, Bjorbaek C, El-Haschimi K, et al. Altered extracellular signal-regulated kinase signaling and glycogen metabolism in skeletal muscle from p90 ribosomal S6 kinase 2 knockout mice. Mol Cell Biol 2001;21:81–87.
59. El-Haschimi K, Dufresne SD, Hirshman MF, Flier JS, Goodyear LJ, Bjorbaek C. Insulin resistance and lipodystrophy in mice lacking ribosomal S6 kinase 2. Diabetes 2003;52:1340–1346.
60. Jacquot S, Zeniou M, Usiello A, et al. Behavior analysis of RSK2 deficient mice: an animal model for the cognitive impairment in the Coffin-Lowry syndrome. Forum European Neuroscience. Paris, 2002 (Abstract).
61. Putz G, Bertolucci F, Raabe T, Zars T, Heisenberg M. The S6KII (rsk) Gene of Drosophila melanogaster differentially affects an operant and a classical learning task. J Neurosci 2004;24:9745–9751.
62. D’Adamo P, Menegon A, Lo Nigro C, et al. Mutations in GDI1 are responsible for X-linked nonspecific mental retardation. Nat Genet 1998;19:134–139.
63. Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 1997;9:496–504.
64. Ishizaki H, Miyoshi J, Kamiya H, et al. Role of Rab GDP dissociation inhibitor alpha in regulating plasticity of hippocampal neurotransmission. Proc Natl Acad Sci USA 2000;97:11,587–11,592.
65. D’Adamo P, Welzl H, Papadimitriou S, et al. Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice. Hum Mol Genet 2002;11:2567–2580.
66. Umbricht D, Vyssotky D, Latanov A, et al. Midlatency auditory event-related potentials in mice: comparison to midlatency auditory ERPs in humans. Brain Res 2004;1019:189–200.
67. D’Adamo P, Meskenaite V, Ziegler U, Wolfer DP, Toniolo D, Lipp H-P. Tracking the roots of human mental retardation: cognitive impairments in Gdi1 knockout mice are associated with anomalous synaptic vesicles. In: Society for Neuroscience, 33rd Annual Meeting, 2003; New Orleans, LA (Abstract).
68. D’Adamo P, Wolfer DP, Kopp C, Tobler I, Toniolo D, Lipp HP. Mice deficient for the synaptic vesicle protein Rab3a show impaired spatial reversal learning and increased explorative activity but none of the behavioral changes shown by mice deficient for the Rab3a regulator Gdi1. Eur J Neurosci 2004;19:1895–1905.
69. Shahbazian MD, Zoghbi HY. Rett syndrome and MeCP2: linking epigenetics and neuronal function. Am J Hum Genet 2002;71:1259–1272.
70. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 2001;27:322–326.
71. Shahbazian M, Young J, Yuva-Paylor L, et al. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 2002;35:243–254.
72. Luikenhuis S, Giacometti E, Beard C, Jaenisch R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc Natl Acad Sci USA 2004;101:6033–6038.
73. Collins AL, Levenson JM, Vilaythong AP, et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 2004;13:2679–2689.
74. Young J, Zoghbi H. X-chromosome inactivation patterns are unbalanced and affect the phenotypic outcome in a mouse model of rett syndrome. Am J Hum Genet 2004;74:511–520.
75. Bienvenu T, Poirier K, Van Esch H, et al. Rare polymorphic variants of the AGTR2 gene in boys with non-specific mental retardation. J Med Genet 2003;40:357–359.
76. Vervoort VS, Beachem MA, Edwards PS, et al. AGTR2 mutations in X-linked mental retardation. Science 2002;296:2401–2403.
77. Ylisaukko-oja T, Rehnstrom K, Vanhala R, Tengstrom C, Lahdetie J, Jarvela I. Identification of two AGTR2 mutations in male patients with non-syndromic mental retardation. Hum Genet 2004;114:211–213.
78. Erdmann J, Dahmlow S, Guse M, Hetzer R, Regitz-Zagrosek V. The assertion that a G21V mutation in AGTR2 causes mental retardation is not supported by other studies. Hum Genet 2004;114:396; author reply, 397.
79. Hein L, Dzau VJ, Barsh GS. Linkage mapping of the angiotensin AT2 receptor gene (Agtr2) to the mouse X chromosome. Genomics 1995;30:369–371.
80. Ichiki T, Labosky PA, Shiota C, et al. Effects on blood pressure and exploratory behaviour of mice lacking angiotensin II type-2 receptor. Nature 1995;377:748–750.
81. Okuyama S, Sakagawa T, Chaki S, Imagawa Y, Ichiki T, Inagami T. Anxiety-like behavior in mice lacking the angiotensin II type-2 receptor. Brain Res 1999;821:150–159.
82. Sakagawa T, Okuyama S, Kawashima N, et al. Pain threshold, learning and formation of brain edema in mice lacking the angiotensin II type 2 receptor. Life Sci 2000;67:2577–2585.
83. Fransen E, Van Camp G, Vits L, Willems PJ. L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Hum Mol Genet 1997;6:1625–1632.
84. Brümmendorf T, Kenwrick S, Rathjen FG. Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr Opin Neurobiol 1998;8:87–97.
85. Welzl H, Stork O. Cell adhesion molecules: key players in memory consolidation? News Physiol Sci 2003;18:147–150.
86. Miller PD, Chung WW, Lagenaur CF, DeKosky ST. Regional distribution of neural cell adhesion molecule (N-CAM) and L1 in human and rodent hippocampus. J Comp Neurol 1993; 327:341–349.
87. Cohen NR, Taylor JS, Scott LB, Guillery RW, Soriano P, Furley AJ. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 1998;8:26–33.
88. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 1997;17:346–349.
89. Demyanenko GP, Tsai AY, Maness PF. Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J Neurosci 1999;19: 4907–4920.
90. Rolf B, Kutsche M, Bartsch U. Severe hydrocephalus in L1-deficient mice. Brain Res 2001;891:247–252.
91. Wiencken-Barger AE, Mavity-Hudson J, Bartsch U, Schachner M, Casagrande VA. The role of L1 in axon pathfinding and fasciculation. Cereb Cortex 2004;14:121–131.
92. Fransen E, D’Hooge R, Van Camp G, et al. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum Mol Genet 1998;7:999–1009.
93. Irintchev A, Koch M, Needham LK, Maness P, Schachner M. Impairment of sensorimotor gating in mice deficient in the cell adhesion molecule L1 or its close homologue, CHL1. Brain Res 2004;1029:131–134.
94. Thelin J, Waldenstrom A, Bartsch U, Schachner M, Schouenborg J. Heat nociception is severely reduced in a mutant mouse deficient for the L1 adhesion molecule. Brain Res 2003;965:75–82.
95. Bliss T, Errington M, Fransen E, et al. Long-term potentiation in mice lacking the neural cell adhesion molecule L1. Curr Biol 2000;10:1607–1610.
96. Law JW, Lee AY, Sun M, et al. Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci 2003;23:10,419–10,432.
97. Wolfer DP, Mohajeri HM, Lipp HP, Schachner M. Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Eur J Neurosci 1998;10:708–717.
98. Kutsche K, Yntema H, Brandt A, et al. Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nat Genet 2000;26:247–250.
99. Kutsche K, Gal A. The mouse Arhgef6 gene: cDNA sequence, expression analysis, and chromosome assignment. Cytogenet Cell Genet 2001;95:196–201.
100. Kohn M, Steinbach P, Hameister H, Kehrer-Sawatzki H. A comparative expression analysis of four MRX genes regulating intracellular signalling via small GTPases. Eur J Hum Genet 2004;12:29–37.
101. Wolfer DP, Kuchenbecker K, Prut L, Neuhaeusser-Wespy F, Kutsche K, Lipp HP. Impaired behavioral control and altered processing of spatial information in mice deficient for the x-chromosomal mental retardation gene Arhgef6. 7th IBANGS meeting, 2005, Sitges, Spain (Abstract).
102. Huttenlocher PR. The neuropathology of phenylketonuria: human and animal studies. Eur J Pediatr 2000;159(Suppl 2):S102–106.
103. Kahler SG, Fahey MC. Metabolic disorders and mental retardation. Am J Med Genet 2003;117C:31–41.
104. McDonald JD, Bode VC, Dove WF, Shedlovsky A. Pahhph-5: a mouse mutant deficient in phenylalanine hydroxylase. Proc Natl Acad Sci USA 1990;87:1965–1967.
105. Shedlovsky A, McDonald JD, Symula D, Dove WF. Mouse models of human phenylketonuria. Genetics 1993;134:1205–1210.
106. Zagreda L, Goodman J, Druin DP, McDonald D, Diamond A. Cognitive deficits in a genetic mouse model of the most common biochemical cause of human mental retardation. J Neurosci 1999;19:6175–6182.
107. Mihalick SM, Langlois JC, Krienke JD, Dube WV. An olfactory discrimination procedure for mice. J Exp Anal Behav 2000;73:305–318.
108. Cabib S, Pascucci T, Ventura R, Romano V, Puglisi-Allegra S. The behavioral profile of severe mental retardation in a genetic mouse model of phenylketonuria. Behav Genet 2003;33:301–310.
109. Ding Z, Harding CO, Thony B. State-of-the-art 2003 on PKU gene therapy. Mol Genet Metab 2004;81:3–8.
110. Mochizuki S, Mizukami H, Ogura T, et al. Long-term correction of hyperphenylalaninemia by AAV-mediated gene transfer leads to behavioral recovery in phenylketonuria mice. Gene Ther 2004;11:1081–1086.
111. Oh HJ, Park ES, Kang S, Jo I, Jung SC. Long-term enzymatic and phenotypic correction in the phenylketonuria mouse model by adeno-associated virus vector-mediated gene transfer. Pediatr Res 2004;56:278–284.
112. Arun D, Gutmann DH. Recent advances in neurofibromatosis type 1. Curr Opin Neurol 2004;17:101–105.
113. Dasgupta B, Gutmann DH. Neurofibromatosis 1: closing the GAP between mice and men. Curr Opin Genet Dev 2003;13:20–27.
114. Costa RM, Silva AJ. Mouse models of neurofibromatosis type I: bridging the GAP. Trends Mol Med 2003;9:19–23.
115. Bernards A, Snijders AJ, Hannigan GE, Murthy AE, Gusella JF. Mouse neurofibromatosis type 1 cDNA sequence reveals high degree of conservation of both coding and non-coding mRNA segments. Hum Mol Genet 1993;2:645–650.
116. Silva AJ, Frankland PW, Marowitz Z, et al. A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat Genet 1997;15:281–284.
117. North K. Neurofibromatosis type 1. Am J Med Genet 2000;97:119–127.
118. Costa RM, Yang T, Huynh DP, et al. Learning deficits, but normal development and tumor predisposition, in mice lacking exon 23a of Nf1. Nat Genet 2001;27:399–405.
119. Costa R, Federov N, Kogan J, et al. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002;415:526–530.
120. Govek EE, Newey SE, Akerman CJ, Cross JR, Van der Veken L, Van Aelst L. The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat Neurosci 2004;7:364–372.
121. Huston JP, Borbely AA. The thalamic rat: general behavior, operant learning with rewarding hypothalamic stimulation, and effects of amphetamine. Physiol Behav 1974;12:433–448.
122. Huston JP, Tomaz C, Fix I. Avoidance learning in rats devoid of the telencephalon plus thalamus. Behav Brain Res 1985;17:87–95.
123. Deacon RM, Croucher A, Rawlins JN. Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behav Brain Res 2002;132:203–213.
124. Balschun D, Wolfer DP, Gass P, et al. Does cAMP response element-binding protein (CREB) have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J Neurosci 2003;23:6304–6314.
125. Wolfer DP, Lipp H-P. Meta-analysis of strategy choice by 85 mutant mouse lines in a standardized place navigation task identifies behavioral flexibility as performance limiting factor. In: Society for Neuroscience, 33rd Annual Meeting, 2003; New Orleans LA (Abstract).
126. Mohajeri MH, Saini K, Li H, et al. Intact spatial memory in mice with seizure-induced partial loss of hippocampal pyramidal neurons. Neurobiol Dis 2003;12:174–181.
127. Galsworthy MJ, Paya-Cano JL, Monleon S, Plomin R. Evidence for general cognitive ability (g) in heterogeneous stock mice and an analysis of potential confounds. Genes Brain Behav 2002; 1:88–95.