Modeling combined schizophrenia-related behavioral and metabolic phenotypes in rodents

Behavioural Brain Research

Volumn 276, Issue , 2015, Pages 130-142

  Sarnyai, Zoltán ^a   Jashar, Cassandra ^a   Olivier, Berend ^b,c,d  

^a JAMES COOK UNIVERSITY   (Australia)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal model; Behavior; Energy metabolism; Phenotype; RDoC; Schizophrenia

Indexed keywords

GLUTAMIC ACID; LEPTIN RECEPTOR; PHENCYCLIDINE;

BEHAVIOR; BEHAVIOR DISORDER; BREEDING; DBA 2 MOUSE; GENE DELETION; KNOCKOUT MOUSE; METABOLIC DISORDER; METABOLIC REGULATION; METABOLISM; MOUSE MUTANT; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PATHOGENESIS; PHENOTYPE; REVIEW; RODENT; RODENT MODEL; SCHIZOPHRENIA; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; GENETICS; MOUSE; PSYCHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; MICE; PHENOTYPE; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 84908570578     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.04.016     Document Type: Review

References (171)

1. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13(10):1161-1169.
2. van den Buuse M. Modeling the positive symptoms of schizophrenia in genetically modified mice: pharmacology and methodology aspects. Schizophr Bull 2010 Mar, 36(2):246-270.
3. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol 2010 Mar, 90(3):285-326.
4. Jones C.A., Watson D.J., Fone K.C. Animal models of schizophrenia. Br J Pharmacol 2011 Oct, 164(4):1162-1194.
5. Arguello P.A., Gogos J.A. Genetic and cognitive windows into circuit mechanisms of psychiatric disease. Trends Neurosci 2012 Jan, 35(1):3-13.
6. Yee B.K., Singer P. A conceptual and practical guide to the behavioural evaluation of animal models of the symptomatology and therapy of schizophrenia. Cell Tissue Res 2013 Oct, 354(1):221-246.
7. Sarnyai Z., Alsaif M., Bahn S., Ernst A., Guest P.C., Hradetzky E., et al. Behavioral and molecular biomarkers in translational animal models for neuropsychiatric disorders. Int Rev Neurobiol 2011, 101:203-238.
8. Insel T., Cuthbert B., Garvey M., Heinssen R., Pine D.S., Quinn K., et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry 2010 Jul, 167(7):748-751.
9. Cuthbert B.N., Insel T.R. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med 2013 May 14, 11:126.
10. van Os J., Kapur S. Schizophrenia. Lancet 2009 Aug 22, 374(9690):635-645.
11. Pokos V., Castle D.J. Prevalence of comorbid anxiety disorders in schizophrenia spectrum disorders: a literature review. Curr Psychiatry Rev 2006, 2:285-307.
12. Achim A.M., Maziade M., Raymond E., Olivier D., Merette C., Roy M.A. How prevalent are anxiety disorders in schizophrenia? A meta-analysis and critical review on a significant association. Schizophr Bull 2011, 37:811-821.
13. Braga R.J., Mendlowicz M.V., Marrocos R.P., Figueira I.L. Anxiety disorders in outpatients with schizophrenia: prevalence and impact on the subjective quality of life. J Psychiatr Res 2005, 39:409-414.
14. Young S., Pfaff D., Lewandowski K.E., Ravichandran C., Cohen B.M., Ongur D. Anxiety disorder comorbidity in bipolar disorder, schizophrenia and schizoaffective disorder. Psychopathology 2012.
15. Hartley S., Barrowclough C., Haddock G. Anxiety and depression in psychosis: a systematic review of associations with positive psychotic symptoms. Acta Psychiatr Scand 2013, 128(5):327-346.
16. Freeman D., Garety P.A. Worry, worry processes and dimensions of delusions: an exploratory investigation of a role for anxiety processes in the maintenance of delusional distress. Behav Cogn Psychother 1999, 27:46-62.
17. Lysaker P.H., Yanos P.T., Outcalt J., Roe D. Association of stigma, self-esteem, and symptoms with concurrent and prospective assessment of social anxiety in schizophrenia. Clin Schizophr Relat Psychoses 2010, 4:41-48.
18. Gard D.E., Fisher M., Garrett C., Genevsky A., Vinogradov S. Motivation and its relationship to neurocognition, social cognition, and functional outcome in schizophrenia. Schizophr Res 2009 Nov, 115(1):74-81.
19. Der-Avakian A., Markou A. The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci 2012 Jan, 35(1):68-77.
20. Ziauddeen H., Murray G.K. The relevance of reward pathways for schizophrenia. Curr Opin Psychiatry 2010 Mar, 23(2):91-96.
21. Braff D.L., Geyer M.A. Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatr 1990, 47:181-188.
22. Hikichi H., Nishino M., Fukushima M., Satow A., Maehara S., Kawamoto H., et al. Pharmacological effects of metabotropic glutamate receptor ligands on prepulse inhibition in DBA/2J mice. Eur J Pharmacol 2010, 639:99-105.
23. Csomor P.A., Yee B.K., Feldon J., Theodoridou A., Studerus E., Vollenweider F.X. Impaired prepulse inhibition and prepulse-elicited reactivity but intact reflex circuit excitability in unmedicated schizophrenia patients: a comparison with healthy subjects and medicated schizophrenia patients. Schizophr Bull 2009, 35:244-255.
24. Braff D.L., Geyer M.A., Light G.A., Sprock J., Perry W., Cadenhead K.S., et al. Impact of prepulse characteristics on the detection of sensorimotor gating deficits in schizophrenia. Schizophr Res 2001, 49:171-178.
25. Grillon C., Ameli R., Charney D.S., Krystal J., Braff D. Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol Psychiatr 1992, 32:939-943.
26. Carter J.D., Bizzell J., Kim C., Bellion C., Carpenter K.L., Dichter G., et al. Attention deficits in schizophrenia-preliminary evidence of dissociable transient and sustained deficits. Schizophr Res 2010, 122:104-112.
27. Anscombe R. The disorder of consciousness in schizophrenia. Schizophr Bull 1987, 13:241-260.
28. Hilti C.C., Delko T., Orosz A.T., Thomann K., Ludewig S., Geyer M.A., et al. Sustained attention and planning deficits but intact attentional set-shifting in neuroleptic-naive first-episode schizophrenia patients. Neuropsychobiology 2010, 61:79-86.
29. Liu S.K., Chiu C.H., Chang C.J., Hwang T.J., Hwu H.G., Chen W.J. Deficits in sustained attention in schizophrenia and affective disorders: stable versus state-dependent markers. Am J Psychiatr 2002, 159:975-982.
30. Tsai J., Lysaker P.H., Vohs J.L. Negative symptoms and concomitant attention deficits in schizophrenia: associations with prospective assessments of anxiety, social dysfunction, and avoidant coping. J Ment Health 2010, 19:184-192.
31. Gjini K., Burroughs S., Boutros N.N. Relevance of attention in auditory sensory gating paradigms in schizophrenia: a pilot study. J Psychophysiol 2011, 25:60-66.
32. Andreasen N.C. Schizophrenia: the fundamental questions. Brain Res Brain Res Rev 2000 Mar, 31(2-3):106-112.
33. Timofeeva O.A., Levin E.D. Glutamate and nicotinic receptor interactions in working memory: importance for the cognitive impairment of schizophrenia. Neuroscience 2011, 195:21-36.
34. He H., Sui J., Yu Q., Turner J.A., Ho B.C., Sponheim S.R., et al. Altered small-world brain networks in schizophrenia patients during working memory performance. PLoS One 2012, 7:e38195.
35. Deserno L., Sterzer P., Wustenberg T., Heinz A., Schlagenhauf F. Reduced prefrontal-parietal effective connectivity and working memory deficits in schizophrenia. J Neurosci 2012, 32:12-20.
36. Kirkpatrick B. Affiliation and neuropsychiatric disorders: the deficit syndrome of schizophrenia. Ann N Y Acad Sci 1997 Jan 15, 807:455-468.
37. Sobin C., Blundell M.L., Conry A., Weiller F., Gavigan C., Haiman C., et al. Early, non-psychotic deviant behavior in schizophrenia: a possible endophenotypic marker for genetic studies. Psychiatry Res 2001 Mar 25, 101(2):101-113.
38. Afonso P., Viveiros V., Vinhas de Sousa T. Sleep disturbances in schizophrenia. Acta Med Port 2011, 24(Suppl 4):799-806.
39. Sarkar S., Katshu M.Z., Nizamie S.H., Praharaj S.K. Slow wave sleep deficits as a trait marker in patients with schizophrenia. Schizophr Res 2010, 124:127-133.
40. Wamsley E.J., Tucker M.A., Shinn A.K., Ono K.E., McKinley S.K., Ely A.V., et al. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation. Biol Psychiatr 2012, 71:154-161.
41. Manoach D.S., Stickgold R. Does abnormal sleep impair memory consolidation in schizophrenia?. Front Hum Neurosci 2009, 3:21.
42. Kaidanovich-Beilin O., Cha D.S., McIntyre R.S. Crosstalk between metabolic and neuropsychiatric disorders. F1000 Biol Rep 2012, 4:14.
43. Meyer J.M., Davis V.G., Goff D.C., McEvoy J.P., Nasrallah H.A., Davis S.M., et al. Change in metabolic syndrome parameters with antipsychotic treatment in the CATIE schizophrenia trial: prospective data from phase 1. Schizophr Res 2008 Apr, 101(1-3):273-286.
44. Ryan M.C., Collins P., Thakore J.H. Impaired fasting glucose tolerance in first-episode, drug-naive patients with schizophrenia. Am J Psychiatry 2003 Feb, 160(2):284-289.
45. Guest P.C., Wang L., Harris L.W., Burling K., Levin Y., Ernst A., et al. Increased levels of circulating insulin-related peptides in first-onset, antipsychotic naïve schizophrenia patients. Mol Psychiatry 2010 Feb, 15(2):118-119.
46. Harris L.W., Guest P.C., Wayland M.T., Umrania Y., Krishnamurthy D., Rahmoune H., et al. Schizophrenia: metabolic aspects of aetiology, diagnosis and future treatment strategies. Psychoneuroendocrinology 2013 Jun, 38(6):752-766.
47. Harris L.W., Pietsch S., Cheng T.M., Schwarz E., Guest P.C., Bahn S. Comparison of peripheral and central schizophrenia biomarker profiles. PLoS One 2012, 7(10):e46368.
48. Du F., Cooper A.J., Thida T., Sehovic S., Lukas S.E., Cohen B.M., et al. In vivo evidence for cerebral bioenergetic abnormalities in schizophrenia measured using 31P magnetization transfer spectroscopy. JAMA Psychiatry 2014 Jan, 71(1):19-27.
49. Voikar V., Polus A., Vasar E., Rauvala H. Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav 2005, 4:240-252.
50. Mozhui K., Karlsson R.M., Kash T.L., Ihne J., Norcross M., Patel S., et al. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 2010, 30:5357-5367.
51. DuBois D.W., Perlegas A., Floyd D.W., Weiner J.L., McCool B.A. Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 2006, 318:629-640.
52. McClearn G.E., Wilson J.R., Meredith W. The use of isogenic and heterogenic mouse stocks in behavioral research. Contribution to behavior genetic analysis. The mouse as a prototype 1970, 3-32. Appleton-Century-Crofts, New York. G. Lindzey, D.D. Thiessen (Eds.).
53. Ammassari-Teule M., Hoffmann H.J., Rossi-Arnaud C. Learning in inbred mice: strain-specific abilities across three radial maze problems. Behav Genet 1993, 23:405-412.
54. Binder E., Malki K., Paya-Cano J.L., Fernandes C., Aitchison K.J., Mathé A.A., et al. Antidepressants and the resilience to early-life stress in inbred mouse strains. Pharmacogenet Genomics 2011 Dec, 21(12):779-789.
55. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 1977, 229:327-336.
56. Sugimoto Y., Kajiwara Y., Hirano K., Yamada S., Tagawa N., Kobayashi Y., et al. Mouse strain differences in immobility and sensitivity to fluvoxamine and desipramine in the forced swimming test: analysis of serotonin and noradrenaline transporter binding. Eur J Pharmacol 2008, 592:116-122.
57. Nikulina E.M., Skrinskaya J.A., Popova N.K. Role of genotype and dopamine receptors in behavior of inbred mice in a forced swimming test. Psychopharmacology 1991, 105:525-529.
58. Freet C.S., Arndt A., Grigson P.S. Compared with DBA/2J mice, C57BL/6J mice demonstrate greater preference for saccharin and less avoidance of a cocaine-paired saccharin cue. Behav Neurosci 2013 Jun, 127(3):474-484.
59. Elmer G.I., Pieper J.O., Hamilton L.R., Wise R.A. Qualitative differences between C57BL/6J and DBA/2J mice in morphine potentiation of brain stimulation reward and intravenous self-administration. Psychopharmacology (Berl) 2010, 208(Feb (2)):309-321.
60. Yoneyama N., Crabbe J.C., Ford M.M., Murillo A., Finn D.A. Voluntary ethanol consumption in 22 inbred mouse strains. Alcohol 2008, 42:149-160.
61. Stolerman I.P., Naylor C., Elmer G.I., Goldberg S.R. Discrimination and self-administration of nicotine by inbred strains of mice. Psychopharmacology (Berl) 1999, 141:297-306.
62. Orsini C., Buchini F., Piazza P.V., Puglisi-Allegra S., Cabib S. Susceptibility to amphetamine-induced place preference is predicted by locomotor response to novelty and amphetamine in the mouse. Psychopharmacology (Berl) 2004, 172:264-270.
63. D'Este L., Casini A., Puglisi-Allegra S., Cabib S., Renda T.G. Comparative immunohistochemical study of the dopaminergic systems in two inbred mouse strains (C57BL/6J and DBA/2J). J Chem Neuroanat 2007, 33:67-74.
64. Olivier B., Leahy C., Mullen T., Paylor R., Groppi V.E., Sarnyai Z., et al. The DBA/2J strain and prepulse inhibition of startle: a model system to test antipsychotics. Psychopharmacology 2001, 156:284-290.
65. Singer P., Feldon J., Yee B.K. Are DBA/2 mice associated with schizophrenia-like endophenotypes? A behavioral contrast with C57BL/6 mice. Psychopharmacology 2009, 206:677-698.
66. Logue S.F., Owen E.H., Rasmussen D.L., Wehner J.M. Assessment of locomotor activity, acoustic and tactile startle, and prepulse inhibition of startle in inbred mouse strains and F1 hybrids: implications of genetic background for single gene and quantitative trait loci analyses. Neuroscience 1997, 80:1075-1086.
67. Yamada K. Strain differences of selective attention in mice: effect of Kamin blocking on classical fear conditioning. Behav Brain Res 2010, 213:126-129.
68. Loos M., Staal J., Schoffelmeer A.N., Smit A.B., Spijker S., Pattij T. Inhibitory control and response latency differences between C57BL/6J and DBA/2J mice in a Go/No-Go and 5-choice serial reaction time task and strain-specific responsivity to amphetamine. Behav Brain Res 2010, 214:216-224.
69. Patel S., Stolerman I.P., Asherson P., Sluyter F. Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task. Behav Brain Res 2006, 170:197-203.
70. Paylor R., Baskall L., Wehner J.M. Behavioral dissociations between C57BL-6 and DBA-2 mice on learning and memory tasks-a hippocampal-dysfunction hypothesis. Psychobiology 1993, 21:11-26.
71. Podhorna J., Brown R.E. Strain differences in activity and emotionality do not account for differences in learning and memory performance between C57BL/6 and DBA/2 mice. Genes Brain Behav 2002, 1:96-110.
72. Nguyen P.V., Abel T., Kandel E.R., Bourtchouladze R. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 2000, 7:170-179.
73. Lattal K.M., Maughan D.K. A parametric analysis of factors affecting acquisition and extinction of contextual fear in C57BL/6 and DBA/2 mice. Behav Process 2012, 90:49-57.
74. Izquierdo A., Wiedholz L.M., Millstein R.A., Yang R.J., Bussey T.J., Saksida L.M., et al. Genetic and dopaminergic modulation of reversal learning in a touchscreen-based operant procedure for mice. Behav Brain Res 2006, 171:181-188.
75. Moy S.S., Nadler J.J., Young N.B., Perez A., Holloway L.P., Barbaro R.P., et al. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 2007 Jan 10, 176(1):4-20.
76. Panksepp J.B., Lahvis G.P. Social reward among juvenile mice. Genes Brain Behav 2007 Oct, 6(7):661-671.
77. Franken P., Malafosse A., Tafti M. Genetic variation in EEG activity during sleep in inbred mice. Am J Physiol 1998, 275:R1127-R1137.
78. Funkat A., Massa C.M., Jovanovska V., Proietto J., Andrikopoulos S. Metabolic adaptations of three inbred strains of mice (C57BL/6, DBA/2, and 129T2) in response to a high-fat diet. J Nutr 2004, 134:3264-3269.
79. Hageman R.S., Wagener A., Hantschel C., Svenson K.L., Churchill G.A., Brockmann G.A. High-fat diet leads to tissue-specific changes reflecting risk factors for diseases in DBA/2J mice. Physiol Genomics 2010, 42:55-66.
80. Tortoriello D.V., McMinn J., Chua S.C. Dietary-induced obesity and hypothalamic infertility in female DBA/2J mice. Endocrinology 2004, 145:1238-1247.
81. Svenson K.L., Von Smith R., Magnani P.A., Suetin H.R., Paigen B., Naggert J.K., et al. Multiple trait measurements in 43 inbred mouse strains capture the phenotypic diversity characteristic of human populations. J Appl Physiol 2007, 102:2369-2378.
82. Atalayer D., Rowland N.E. Comparison of C57BL/6 and DBA/2 mice in food motivation and satiety. Physiol Behav 2010, 99:679-683.
83. Alexander J., Chang G.Q., Dourmashkin J.T., Leibowitz S.F. Distinct phenotypes of obesity-prone AKR/J, DBA2J and C57BL/6J mice compared to control strains. Int J Obes 2006, 30:50-59.
84. Leung H.W., Ku R.H., Paustenbach D.J., Andersen M.E. A physiologically based pharmacokinetic model for 2,3,7,8-tetrachlorodibenzo-p-dioxin in C57BL/6J and DBA/2J mice. Toxicol Lett 1988, 42:15-28.
85. Ahotupa M., Mantyla E. Adipose tissue content as a modifier of the tissue distribution, biological effects, and excretion of a hexachlorobiphenyl in C57BL/6J and DBA/JBOMf mice. Mol Pharmacol 1983, 24:464-470.
86. Hempenstall S., Picchio L., Mitchell S.E., Speakman J.R., Selman C. The impact of acute caloric restriction on the metabolic phenotype in male C57BL/6 and DBA/2 mice. Mech Ageing Dev 2010, 131:111-118.
87. Berglund E.D., Li C.Y., Poffenberger G., Ayala J.E., Fueger P.T., Willis S.E., et al. Glucose metabolism in vivo in four commonly used inbred mouse strains. Diabetes 2008, 57:1790-1799.
88. Goren H.J., Kulkarni R.N., Kahn C.R. Glucose homeostasis and tissue transcript content of insulin signaling intermediates in four inbred strains of mice: C57BL/6, C57BLKS/6, DBA/2, and 129X1. Endocrinology 2004, 145:3307-3323.
89. Gurley S.B., Clare S.E., Snow K.P., Hu A., Meyer T.W., Coffman T.M. Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 2006, 290:F214-F222.
90. Chen H., Charlat O., Tartaglia L.A., Woolf E.A., Weng X., Ellis S.J., et al. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996, 84:491-495.
91. Hummel K.P., Dickie M.M., Coleman D.L. Diabetes, a new mutation in the mouse. Science 1966, 153:1127-1128.
92. Dinel A.L., Andre C., Aubert A., Ferreira G., Laye S., Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One 2011, 6:e24325.
93. Sharma A.N., Elased K.M., Garrett T.L., Lucot J.B. Neurobehavioral deficits in db/db diabetic mice. Physiol Behav 2010, 101:381-388.
94. Blednov Y.A., Walker D., Harris R.A. Blockade of the leptin-sensitive pathway markedly reduces alcohol consumption in mice. Alcohol Clin Exp Res 2004 Nov, 28(11):1683-1692.
95. Oomura Y., Aou S., Fukunaga K. Prandial increase of leptin in the brain activates spatial learning and memory. Pathophysiology 2010, 17:119-127.
96. Li X.L., Aou S., Oomura Y., Hori N., Fukunaga K., Hori T. Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience 2002, 113:607-615.
97. Ohta R., Shigemura N., Sasamoto K., Koyano K., Ninomiya Y. Conditioned taste aversion learning in leptin-receptor-deficient db/db mice. Neurobiol Learn Mem 2003, 80:105-112.
98. Laposky A.D., Bradley M.A., Williams D.L., Bass J., Turek F.W. Sleep-wake regulation is altered in leptin-resistant (db/db) genetically obese and diabetic mice. Am J Physiol Regul Integr Comp Physiol 2008 Dec, 295(6):R2059-R2066.
99. Kodama H., Fujita M., Yamaguchi I. Development of hyperglycaemia and insulin resistance in conscious genetically diabetic (C57BL/KsJ-db/db) mice. Diabetologia 1994, 37:739-744.
100. Edgel K.A., McMillen T.S., Wei H., Pamir N., Houston B.A., Caldwell M.T., et al. Obesity and weight loss result in increased adipose tissue ABCG1 expression in db/db mice. Biochim Biophys Acta 2012, 1821:425-434.
101. Schroeder-Gloeckler J.M., Rahman S.M., Janssen R.C., Qiao L., Shao J., Roper M., et al. CCAAT/enhancer-binding protein beta deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. J Biol Chem 2007, 282:15717-15729.
102. Demarco V.G., Ford D.A., Henriksen E.J., Aroor A.R., Johnson M.S., Habibi J., et al. Obesity-related alterations in cardiac lipid profile and nondipping blood pressure pattern during transition to diastolic dysfunction in male db/db mice. Endocrinology 2013, 154:159-171.
103. Davis R.C., Castellani L.W., Hosseini M., Ben-Zeev O., Mao H.Z., Weinstein M.M., et al. Early hepatic insulin resistance precedes the onset of diabetes in obese C57BLKS-db/db mice. Diabetes 2010, 59:1616-1625.
104. Ernst A., Sharma A.N., Elased K.M., Guest P.C., Rahmoune H., Bahn S. Diabetic db/db mice exhibit central nervous system and peripheral molecular alterations as seen in neurological disorders. Transl Psychiatry 2013, 3:e263.
105. Kirov G., Pocklington A.J., Holmans P., Ivanov D., Ikeda M., Ruderfer D., et al. De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 2012, 17:142-153.
106. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008, 320:539-543.
107. Kristiansen L.V., Beneyto M., Haroutunian V., Meador-Woodruff J.H. Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia. Mol Psychiatry 2006, 11:737-747.
108. Carlisle H.J., Fink A.E., Grant S.G., O'Dell T.J. Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J Physiol 2008, 586:5885-5900.
109. Nithianantharajah J., Komiyama N.H., McKechanie A., Johnstone M., Blackwood D.H., St Clair D., et al. Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nat Neurosci 2013, 16:16-24.
110. Palmer N.D., Mychaleckyj J.C., Langefeld C.D., Ziegler J.T., Williams A.H., Bryer-Ash M., et al. Evaluation of DLG2 as a positional candidate for disposition index in African-Americans from the IRAS family study. Diab Res Clin Pract 2010, 87:69-76.
111. Brown A.S. The environment and susceptibility to schizophrenia. Prog Neurobiol 2011 Jan, 93(1):23-58.
112. Hoek H.W., Brown A.S., Susser E. The Dutch famine and schizophrenia spectrum disorders. Soc Psychiatry Psychiatr Epidemiol 1998, 33:373-379.
113. St Clair D., Xu M., Wang P., Yu Y., Fang Y., Zhang F., et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 2005, 294:557-562.
114. Reyes-Castro L.A., Rodriguez J.S., Charco R., Bautista C.J., Larrea F., Nathanielsz P.W., et al. Maternal protein restriction in the rat during pregnancy and/or lactation alters cognitive and anxiety behaviors of female offspring. Int J Dev Neurosci 2012 Feb, 30(1):39-45.
115. Reyes-Castro L.A., Rodriguez J.S., Rodríguez-González G.L., Chavira R., Bautista C.J., McDonald T.J., et al. Pre- and/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats. Behav Brain Res 2012 Feb 14, 227(2):324-329.
116. Reyes-Castro L.A., Rodriguez J.S., Rodríguez-González G.L., Wimmer R.D., McDonald T.J., Larrea F., et al. Pre- and/or postnatal protein restriction in rats impairs learning and motivation in male offspring. Int J Dev Neurosci 2011 Apr, 29(2):177-182.
117. da Silva A.A., Borba T.K., de Almeida Lira L., Cavalcante T.C., de Freitas M.F., Leandro C.G., et al. Perinatal undernutrition stimulates seeking food reward. Int J Dev Neurosci 2013 Aug, 31(5):334-341.
118. Vucetic Z., Totoki K., Schoch H., Whitaker K.W., Hill-Smith T., Lucki I., et al. Early life protein restriction alters dopamine circuitry. Neuroscience 2010 Jun 30, 168(2):359-370.
119. Palmer A.A., Printz D.J., Butler P.D., Dulawa S.C., Printz M.P. Prenatal protein deprivation in rats induces changes in prepulse inhibition and NMDA receptor binding. Brain Res 2004, 996:193-201.
120. Austin K.B., Bronzino J., Morgane P.J. Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Res 1986, 394:267-273.
121. Ozanne S.E., Nave B.T., Wang C.L., Shepherd P.R., Prins J., Smith G.D. Poor fetal nutrition causes long-term changes in expression of insulin signaling components in adipocytes. Am J Physiol 1997, 273:E46-E51.
122. Petry C.J., Dorling M.W., Pawlak D.B., Ozanne S.E., Hales C.N. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diab Res 2001, 2:139-143.
123. Ozanne S.E., Olsen G.S., Hansen L.L., Tingey K.J., Nave B.T., Wang C.L., et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol 2003, 177:235-241.
124. Guest P.C., Urday S., Ma D., Stelzhammer V., Harris L.W., Amess B., et al. Proteomic analysis of the maternal protein restriction rat model for schizophrenia: identification of translational changes in hormonal signaling pathways and glutamate neurotransmission. Proteomics 2012, 12:3580-3589.
125. Javitt D.C., Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 1991, 148:1301-1308.
126. Javitt D.C. Glutamate and schizophrenia: phencyclidine, N-methyl-D-aspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol 2007, 78:69-108.
127. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., et al. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol Ther 2010 Dec, 128(3):419-432.
128. Adell A., Jiménez-Sánchez L., López-Gil X., Romón T. Is the acute NMDA receptor hypofunction a valid model of schizophrenia?. Schizophr Bull 2012, 38:9-14.
129. Wang C., McInnis J., Ross-Sanchez M., Shinnick-Gallagher P., Wiley J.L., Johnson K.M. Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 2001, 107:535-550.
130. Ernst A., Ma D., Garcia-Perez I., Tsang T.M., Kluge W., Schwarz E., et al. Molecular validation of the acute phencyclidine rat model for schizophrenia: identification of translational changes in energy metabolism and neurotransmission. J Prot Res 2012, 11:3704-3714.
131. Murray T.F., Horita A. Phencyclidine-induced stereotyped behavior in rats: dose response effects and antagonism by neuroleptics. Life Sci 1979, 24:2217-2225.
132. Verebey K., Kogan M.J., Mule S.J. Phencyclidine-induced stereotype in rats: effects of methadone, apomorphine, and naloxone. Psychopharmacology 1981, 75:44-47.
133. Enkel T., Thomas M., Bartsch D. Differential effects of subchronic phencyclidine on anxiety in the light-enhanced startle-, light/dark exploration- and open field tests. Behav Brain Res 2013 Apr 15, 243:61-65.
134. McLean S.L., Woolley M.L., Neill J.C. Effects of subchronic phencyclidine on behaviour of female rats on the elevated plus maze and open field. J Psychopharmacol 2010 May, 24(5):787-790.
135. Turgeon S.M., Kim D., Pritchard M., Salgado S., Thaler A. The effects of phencyclidine (PCP) on anxiety-like behavior in the elevated plus maze and the light-dark exploration test are age dependent, sexually dimorphic, and task dependent. Pharmacol Biochem Behav 2011 Nov, 100(1):191-198.
136. Noda Y., Yamada K., Furukawa H., Nabeshima T. Enhancement of immobility in a forced swimming test by subacute or repeated treatment with phencyclidine: a new model of schizophrenia. Br J Pharmacol 1995, 116:2531-2537.
137. Jentsch J.D., Taylor J.R. Impaired inhibition of conditioned responses produced by subchronic administration of phencyclidine to rats. Neuropsychopharmacology 2001 Jan, 24(1):66-74.
138. Turgeon S.M., Hoge S.G. Prior exposure to phencyclidine decreases voluntary sucrose consumption and operant performance for food reward. Pharmacol Biochem Behav 2003 Dec, 76(3-4):393-400.
139. Spielewoy C., Markou A. Withdrawal from chronic phencyclidine treatment induces long-lasting depression in brain reward function. Neuropsychopharmacology 2003 Jun, 28(6):1106-1116.
140. Lydall E.S., Gilmour G., Dwyer D.M. Analysis of licking microstructure provides no evidence for a reduction in reward value following acute or sub-chronic phencyclidine administration. Psychopharmacology (Berl) 2010, 209(Apr (2)):153-162.
141. Spano M.S., Fadda P., Frau R., Fattore L., Fratta W. Cannabinoid self-administration attenuates PCP-induced schizophrenia-like symptoms in adult rats. Eur Neuropsychopharmacol 2010, 20:25-36.
142. Kesner R.P., Dakis M. Phencyclidine disrupts acquisition and retention performance within a spatial continuous recognition memory task. Pharmacol Biochem Behav 1993, 44:419-424.
143. Ma J., Shen B., Rajakumar N., Leung L.S. The medial septum mediates impairment of prepulse inhibition of acoustic startle induced by a hippocampal seizure or phencyclidine. Behav Brain Res 2004, 155:153-166.
144. Keith V.A., Mansbach R.S., Geyer M.A. Failure of haloperidol to block the effects of phencyclidine and dizocilpine on prepulse inhibition of startle. Biol Psychiatr 1991, 30:557-566.
145. Bakshi V.P., Geyer M.A. Phencyclidine-induced deficits in prepulse inhibition of startle are blocked by prazosin, an alpha-1 noradrenergic antagonist. J Pharmacol Exp Ther 1997, 283:666-674.
146. Geyer M.A., Segal D.S., Greenberg B.D. Increased startle responding in rats treated with phencyclidine. Neurobehav Toxicol Teratol 1984, 6:161-164.
147. Mansbach R.S., Geyer M.A. Effects of phencyclidine and phencyclidine biologs on sensorimotor gating in the rat. Neuropsychopharmacology 1989, 2:299-308.
148. Sams-Dodd F. Distinct effects of d-amphetamine and phencyclidine on the social behaviour of rats. Behav Pharmacol 1995, 6:55-65.
149. Steinpreis R.E., Sokolowski J.D., Papanikolaou A., Salamone J.D. The effects of haloperidol and clozapine on PCP- and amphetamine-induced suppression of social behavior in the rat. Pharmacol Biochem Behav 1994, 47:579-585.
150. Sebban C., Tesolin-Decros B., Ciprian-Ollivier J., Perret L., Spedding M. Effects of phencyclidine (PCP) and MK 801 on the EEGq in the prefrontal cortex of conscious rats; antagonism by clozapine, and antagonists of AMPA-, alpha(1)- and 5-HT(2A)-receptors. Br J Pharmacol 2002 Jan, 135(1):65-78.
151. Phillips K.G., Cotel M.C., McCarthy A.P., Edgar D.M., Tricklebank M., O'Neill M.J., et al. Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 2012 Mar, 62(3):1359-1370.
152. Gao X.M., Shirakawa O., Du F., Tamminga C.A. Delayed regional metabolic actions of phencyclidine. Eur J Pharmacol 1993, 241:7-15.
153. Iltis I., Koski D.M., Eberly L.E., Nelson C.D., Deelchand D.K., Valette J., et al. Neurochemical changes in the rat prefrontal cortex following acute phencyclidine treatment: an in vivo localized (1)H MRS study. NMR Biomed 2009, 22:737-744.
154. Martins-de-Souza D., Alsaif M., Ernst A., Harris L.W., Aerts N., Lenaerts I., et al. The application of selective reaction monitoring confirms dysregulation of glycolysis in a preclinical model of schizophrenia. BMC Res Notes 2012, 5:146.
155. Wesseling H., Chan M.K., Tsang T.M., Ernst A., Peters F., Guest P.C., et al. A combined metabonomic and proteomic approach identifies frontal cortex changes in a chronic phencyclidine rat model in relation to human schizophrenia brain pathology. Neuropsychopharmacology 2013 Nov, 38(12):2532-2544.
156. Francis H., Stevenson R. The longer-term impacts of Western diet on human cognition and the brain. Appetite 2013 Apr, 63:119-128.
157. Labouesse M.A., Stadlbauer U., Langhans W., Meyer U. Chronic high fat diet consumption impairs sensorimotor gating in mice. Psychoneuroendocrinology 2013 Nov, 38(11):2562-2574.
158. McNay E.C., Ong C.T., McCrimmon R.J., Cresswell J., Bogan J.S., Sherwin R.S. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem 2010, 93:546-553.
159. Franken P., Gip P., Hagiwara G., Ruby N.F., Heller H.C. Changes in brain glycogen after sleep deprivation vary with genotype. Am J Physiol Regul Integr Comp Physiol 2003, 285:R413-R419.
160. Sharma A.N., Elased K.M., Lucot J.B. Rosiglitazone treatment reversed depression- but not psychosis-like behavior of db/db diabetic mice. J Psychopharmacol 2012, 26:724-732.
161. Mcintyre R.S., Soczynska J.K., Lewis G.F., Macqueen G.M., Konarski J.Z., Kennedy S.H. Managing psychiatric disorders with antidiabetic agents: translational research and treatment opportunities. Expert Opin Pharmacother 2006, 7:1305-1321.
162. Stone W.S., Hsi X. Declarative memory deficits and schizophrenia: problems and prospects. Neurobiol Learn Mem 2011, 96:544-552.
163. Ott V., Benedict C., Schultes B., Born J., Hallschmid M. Intranasal administration of insulin to the brain impacts cognitive function and peripheral metabolism. Diab Obes 2012, 14:214-221.
164. Emamian E.S. AKT/GSK3 signaling pathway and schizophrenia. Front Mol Neurosci 2012, 5:33.
165. Eldar-Finkelman H., Martinez A. GSK-3 inhibitors: preclinical and clinical focus on CNS. Front Mol Neurosci 2011, 4:32.
166. Rolland B., Marche K., Cottencin O., Bordet R. The PPARalpha agonist fenofibrate reduces prepulse inhibition disruption in a neurodevelopmental model of schizophrenia. Schizophr Res Treatment 2012, 2012:839853.
167. Pipatpiboon N., Pratchayasakul W., Chattipakorn N., Chattipakorn S.C. PPARgamma agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term high-fat diets. Endocrinology 2012, 153:329-338.
168. Ryan C.M., Freed M.I., Rood J.A., Cobitz A.R., Waterhouse B.R., Strachan M.W. Improving metabolic control leads to better working memory in adults with type 2 diabetes. Diab Care 2006, 29:345-351.
169. Mitchell A.J., Dinan T.G. Schizophrenia: a multisystem disease?. J Psychopharmacol 2010 Nov, 24(Suppl 4):5-7.
170. Steiner J., Bernstein H.G., Schiltz K., Müller U.J., Westphal S., Drexhage H.A., et al. Immune system and glucose metabolism interaction in schizophrenia: a chicken-egg dilemma. Prog Neuropsychopharmacol Biol Psychiatry 2014 Jan 3, 48:287-294.
171. Kalueff A.V., Stewart A.M. Modeling neuropsychiatric spectra to empower translational biological psychiatry. Behav Brain Res 2014, 276:1-7.