Characterization of gene-environment interactions by behavioral profiling of selectively bred rats: The effect of NMDA receptor inhibition and social isolation

Behavioural Brain Research

Volumn 240, Issue 1, 2013, Pages 134-145

  Petrovszki, Zita ^a   Adam, Gabor ^a   Tuboly, Gabor ^b   Kekesi, Gabriella ^a   Benedek, Gyorgy ^a   Keri, Szabolcs ^a   Horvath, Gyongyi ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Memory; Motor behavior; Pain; Prepulse inhibition; Schizophrenia; Selective breeding

Indexed keywords

KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREEDING METHOD; DECLARATIVE MEMORY; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE ENVIRONMENT INTERACTION; GROOMING; HABITUATION; LATENT PERIOD; MALE; MEMORY DISORDER; MOTOR ACTIVITY; NONHUMAN; PAIN THRESHOLD; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; RAT STRAIN; RECOGNITION; SCHIZOPHRENIA; SENSORY GATING; SOCIAL ISOLATION; STARTLE REFLEX; TAIL FLICK TEST;

ACOUSTIC STIMULATION; ANIMALS; BEHAVIOR, ANIMAL; BREEDING; DISEASE MODELS, ANIMAL; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; KETAMINE; MALE; PAIN THRESHOLD; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SOCIAL ISOLATION; STARTLE REACTION;

EID: 84871399704     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.11.022     Document Type: Article

References (121)

1. Rossler W., Joachim Salize H., van Os J., Riecher-Rossler A. Size of burden of schizophrenia and psychotic disorders. European Neuropsychopharmacology 2005, 15:399-409.
2. Insel T.R. Rethinking schizophrenia. Nature 2010, 468:187-193.
3. Cohen-Woods S., Schosser A., McGuffin P. From age correction to genome-wide association. Acta Psychiatrica Scandinavica 2009, 120:355-362.
4. Ayhan Y., Sawa A., Ross C.A., Pletnikov M.V. Animal models of gene-environment interactions in schizophrenia. Behavioural Brain Research 2009, 204:274-281.
5. Nagai T., Ibi D., Yamada K. Animal model for schizophrenia that reflects gene-environment interactions. Biological and Pharmaceutical Bulletin 2011, 34:1364-1368.
6. Tuboly G., Benedek G., Horvath G. Selective disturbance of pain sensitivity after social isolation. Physiology and Behavior 2009, 96:18-22.
7. Chen J., Lipska B.K., Weinberger D.R. Genetic mouse models of schizophrenia: from hypothesis-based to susceptibility gene-based models. Biological Psychiatry 2006, 59:1180-1188.
8. Weiss I.C., Feldon J. Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 2001, 156:305-326.
9. Arranz M.J., de Leon J. Pharmacogenetics and pharmacogenomics of schizophrenia: a review of last decade of research. Molecular Psychiatry 2007, 12:707-747.
10. Linn G.S., O'Keeffe R.T., Schroeder C.E., Lifshitz K., Javitt D.C. Behavioral effects of chronic phencyclidine in monkeys. NeuroReport 1999, 10:2789-2793.
11. Geyer M.A., Krebs-Thomson K., Braff D.L., Swerdlow N.R. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001, 156:117-154.
12. Swerdlow N.R., Geyer M.A., Shoemaker J.M., Light G.A., Braff D.L., Stevens K.E., et al. Convergence and divergence in the neurochemical regulation of prepulse inhibition of startle and N40 suppression in rats. Neuropsychopharmacology 2006, 31:506-515.
13. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20:201-225.
14. 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. Journal of Psychopharmacology 2009, 1-4.
15. Kekesi O., Tuboly G., Szucs M., Birkas E., Morvay Z., Benedek G., et al. Long-lasting, distinct changes in central opioid receptor and urinary bladder functions in models of schizophrenia in rats. European Journal of Pharmacology 2011, 661:35-41.
16. Wong A.H.C., Van Tol H.H.M. Schizophrenia: from phenomenology to neurobiology. Neuroscience and Biobehavioral Reviews 2003, 27:269-306.
17. Egerton A., Reid L., McGregor S., Cochran S.M., Morris B.J., Pratt J.A. Subchronic and chronic PCP treatment produces temporally distinct deficits in attentional set shifting and prepulse inhibition in rats. Psychopharmacology 2008, 198:37-49.
18. Breese G.R., Knapp D.J., Moy S.S. Integrative role for serotonergic and glutamatergic receptor mechanisms in the action of NMDA antagonists: potential relationships to antipsychotic drug actions on NMDA antagonist responsiveness. Neuroscience and Biobehavioral Reviews 2002, 26:441-455.
19. Li J.T., Su Y.A., Guo C.M., Feng Y., Yang Y., Huang R.H., et al. Persisting cognitive deficits induced by low-dose, subchronic treatment with MK-801 in adolescent rats. European Journal of Pharmacology 2011, 652:65-72.
20. Nemeth H., Varga H., Farkas T., Kis Z., Vecsei L., Horvath S., et al. Long-term effects of neonatal MK-801 treatment on spatial learning and cortical plasticity in adult rats. Psychopharmacology 2002, 160:1-8.
21. Kawabe K., Iwasaki T., Ichitani Y. Repeated treatment with N-methyl-d-aspartate antagonists in neonatal, but not adult, rats causes long-term deficits of radial-arm maze learning. Brain Research 2007, 1169:77-86.
22. Rujescu D., Bender A., Keck M., Hartmann A.M., Ohl F., Raeder H., et al. A Pharmacological model for psychosis based on N-methyl-d-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities. Biological Psychiatry 2006, 59:721-729.
23. Huang B.S., Leenen F.H.H. Mineralocorticoid actions in the brain and hypertension. Current Hypertension Reports 2011, 13:214-220.
24. Keilhoff G., Becker A., Grecksch G., Wolf G., Bernstein H.G. Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 2004, 126:591-598.
25. Woo T.U.W., Crowell A.L. Targeting synapses and myelin in the prevention of schizophrenia. Schizophrenia Research 2005, 73:193-207.
26. Hatch A.M., Wiberg G.S., Zawidzka Z., Cann M., Airth J.M., Grice H.C. Isolation syndrome in the rat. Toxicology and Applied Pharmacology 1965, 7:737-745.
27. Grippo A.J., Trahanas D.M., Zimmerman II.R.R, Porges S.W., Carter C.S. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 2009, 34:1542-1553.
28. Grippo A.J., Lamb D.G., Carter C.S., Porges S.W. Social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors. Biological Psychiatry 2007, 62:1162-1170.
29. Puglisi-Allegra S., Oliverio A. Social isolation: effects on pain threshold and stress-induced analgesia. Pharmacology Biochemistry and Behavior 1983, 19:679-681.
30. Fabricius K., Steiniger-Brach B., Helboe L., Fink-Jensen A., Wortwein G. Socially isolated rats exhibit changes in dopamine homeostasis pertinent to schizophrenia. International Journal of Developmental Neuroscience 2011, 29:347-350.
31. Fone K.C.F., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neuroscience and Biobehavioral Reviews 2008, 32:1087-1102.
32. Lapiz M.D.S., Fulford A., Muchimapura S., Mason R., Parker T., Marsden C.A. Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neuroscience and Behavioral Physiology 2003, 33:13-29.
33. Fulford A.J., Marsden C.A. An intact dopaminergic system is required for context-conditioned release of 5-HT in the nucleus accumbens of postweaning isolation-reared rats. Neuroscience 2007, 149:392-400.
34. Djouma E., Card K., Lodge D.J., Lawrence A.J. The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D-2 receptors in the amygdala and nucleus accumbens of Fawn-Hooded rats. European Journal of Neuroscience 2006, 23:3319-3327.
35. Hickey A.J., Reynolds J.N., Beninger R.J. Post-weaning social isolation and subchronic NMDA glutamate receptor blockade: effects on locomotor activity and GABA signaling in the rat suggest independent mechanisms. Pharmacology Biochemistry and Behavior 2012, 101:231-238.
36. Ashby D.M., Habib D., Dringenberg H.C., Reynolds J.N., Beninger R.J. Subchronic MK-801 treatment and post-weaning social isolation in rats: differential effects on locomotor activity and hippocampal long-term potentiation. Behavioural Brain Research 2010, 212:64-70.
37. Becker A., Grecksch G., Zernig G., Ladstaetter E., Hiemke C., Schmitt U. Haloperidol and risperidone have specific effects on altered pain sensitivity in the ketamine model of schizophrenia. Psychopharmacology 2009, 202:579-587.
38. Becker A., Grecksch G., Schroder H. Pain sensitivity is altered in animals after subchronic ketamine treatment. Psychopharmacology 2006, 189:237-247.
39. Gibbs A.G. Laboratory selection for the comparative physiologist. Journal of Experimental Biology 1999, 202:2709-2718.
40. Touma C., Bunck M., Glasl L., Nussbaumer M., Palme R., Stein H., et al. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 2008, 33:839-862.
41. Smits B.M.G., Peters T.A., Mul J.D., Croes H.J., Fransen J.A.M., Beynon A.J., et al. Identification of a rat model for usher syndrome type 1B by N-ethyl-N-nitrosourea mutagenesis-driven forward genetics. Genetics 2005, 170:1887-1896.
42. Stead J., Clinton S., Neal C., Schneider J., Jama A., Miller S., et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behavior Genetics 2006, 36:697-712.
43. Dieckmann M., Freudenberg F., Klein S., Koch M., Schwabe K. Disturbed social behavior and motivation in rats selectively bred for deficient sensorimotor gating. Schizophrenia Research 2007, 97:250-253.
44. Becker A., Grecksch G. Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Test of predictive validity. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2004, 28:1267-1277.
45. Barr A.M., Powell S.B., Markou A., Geyer M.A. Iloperidone reduces sensorimotor gating deficits in pharmacological models, but not a developmental model, of disrupted prepulse inhibition in rats. Neuropharmacology 2006, 51:457-465.
46. Ognibene E., Adriani W., Macri S., Laviola G. Neurobehavioural disorders in the infant reeler mouse model: interaction of genetic vulnerability and consequences of maternal separation. Behavioural Brain Research 2007, 177:142-149.
47. Laviola G., Ognibene E., Romano E., Adriani W., Keller F. Gene-environment interaction during early development in the heterozygous reeler mouse: clues for modelling of major neurobehavioral syndromes. Neuroscience and Biobehavioral Reviews 2009, 33:560-572.
48. Swerdlow N.R., Geyer M.A., Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology 2001, 156:194-215.
49. Moriwaki M., Kishi T., Takahashi H., Hashimoto R., Kawashima K., Okochi T., et al. Prepulse inhibition of the startle response with chronic schizophrenia: a replication study. Neuroscience Research 2009, 65:259-262.
50. Ludewig K., Geyer M.A., Etzensberger M., Vollenweider F.X. Stability of the acoustic startle reflex, prepulse inhibition, and habituation in schizophrenia. Schizophrenia Research 2002, 55:129-137.
51. Braff D.L., Geyer M.A. Sensorimotor gating and schizophrenia: human and animal model studies. Archives of General Psychiatry 1990, 47:181-188.
52. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 2001, 156:234-258.
53. Boctor S.Y., Ferguson S.A. Neonatal NMDA receptor antagonist treatments have no effects on prepulse inhibition of postnatal day 25 Sprague-Dawley rats. Neurotoxicology 2009, 30:151-154.
54. Takahashi M., Kakita A., Futamura T., Watanabe Y., Mizuno M., Sakimura K., et al. Sustained brain-derived neurotrophic factor up-regulation and sensorimotor gating abnormality induced by postnatal exposure to phencyclidine: comparison with adult treatment. Journal of Neurochemistry 2006, 99:770-780.
55. Su Y.A., Wang X.D., Li J.T., Guo C.M., Feng Y., Yang Y., et al. Age-specific effects of early MK-801 treatment on working memory in female rats. NeuroReport 2011, 22:402-406.
56. Wedzony K., Fijal K., Mackowiak M., Chocyk A., Zajaczkowski W. Impact of postnatal blockade of N-methyl-d-aspartate receptors on rat behavior: a search for a new developmental model of schizophrenia. Neuroscience 2008, 153:1370-1379.
57. Becker A., Peters B., Schroeder H., Mann T., Huether G., Grecksch G. Ketamine-induced changes in rat behaviour: a possible animal model of schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27:687-700.
58. Martinez Z.A., Ellison G.D., Geyer M.A., Swerdlow N.R. Effects of sustained phencyclidine exposure on sensorimotor gating of startle in rats. Neuropsychopharmacology 1999, 21:28-39.
59. Tunstall B., Beckett S., Mason R. Ultrasonic vocalisations explain unexpected effects on pre-pulse inhibition responses in rats chronically pre-treated with phencyclidine. Behavioural Brain Research 2009, 202:184-191.
60. Weiss I.C., Pryce C.R., Jongen-Relo A.L., Nanz-Bahr N.I., Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behavioural Brain Research 2004, 152:279-295.
61. Li N., Ping J., Wu R., Wang C., Wu X., Li L. Auditory fear conditioning modulates prepulse inhibition in socially reared rats and isolation-reared rats. Behavioral Neuroscience 2008, 122:107-118.
62. Varty G.B., Powell S.B., Lehmann-Masten V., Buell M.R., Geyer M.A. Isolation rearing of mice induces deficits in prepulse inhibition of the startle response. Behavioural Brain Research 2006, 169:162-167.
63. Varty G.B., Paulus M.P., Braff D.L., Geyer M.A. Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity. Biological Psychiatry 2000, 47:864-873.
64. Rosa M.L.N.M., Silva R.C.B., Moura-de-Carvalho F.T., Brandao M.L., Guimaraes F.S., Del Bel E.A. Routine post-weaning handling of rats prevents isolation rearing-induced deficit in prepulse inhibition. Brazilian Journal of Medical and Biological Research 2005, 38:1691-1696.
65. Cilia J., Cluderay J.E., Robbins M.J., Reavill C., Southam E., Kew J.N.C., et al. Reversal of isolation-rearing-induced PPI deficits by an alpha 7 nicotinic receptor agonist. Psychopharmacology 2005, 182:214-219.
66. Cilia J., Reavill C., Hagan J.J., Jones D.N.C. Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats. Psychopharmacology 2001, 156:327-337.
67. Heidbreder C.A., Foxton R., Cilia J., Hughes Z.A., Shah A.J., Atkins A., et al. Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology 2001, 156:338-351.
68. Varty G.B., Braff D.L., Geyer M.A. Is there a critical developmental 'window' for isolation rearing-induced changes in prepulse inhibition of the acoustic startle response?. Behavioural Brain Research 1999, 100:177-183.
69. Weiss I.C., Domeney A.M., Moreau J.L., Russig H., Feldon J. Dissociation between the effects of pre-weaning and/or post-weaning social isolation on prepulse inhibition and latent inhibition in adult Sprague-Dawley rats. Behavioural Brain Research 2001, 121:207-218.
70. Freudenberg F., Dieckmann M., Winter S., Koch M., Schwabe K. Selective breeding for deficient sensorimotor gating is accompanied by increased perseveration in rats. Neuroscience 2007, 148:612-622.
71. Hadamitzky M., Harich S., Koch M., Schwabe K. Deficient prepulse inhibition induced by selective breeding of rats can be restored by the dopamine D2 antagonist haloperidol. Behavioural Brain Research 2007, 177:364-367.
72. Schwabe K., Polikashvili N., Krauss J.K. Deficient sensorimotor gating induced by selective breeding in rats is improved by entopeduncular nucleus lesions. Neurobiology of Disease 2009, 34:351-356.
73. Schwabe K., Freudenberg F., Koch M. Selective breeding of reduced sensorimotor gating in Wistar rats. Behavior Genetics 2007, 37:706-712.
74. Eells J.B., Misler J.A., Nikodem V.M. Early postnatal isolation reduces dopamine levels, elevates dopamine turnover and specifically disrupts prepulse inhibition in Nurr1-null heterozygous mice. Neuroscience 2006, 140:1117-1126.
75. Lewis D.A., Cho R.Y., Carter C.S., Eklund K., Forster S., Kelly M.A., et al. Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia. American Journal of Psychiatry 2008, 165:1585-1593.
76. Keri S., Seres I., Kelemen O., Benedek G. Neuregulin 1-stimulated phosphorylation of AKT in psychotic disorders and its relationship with neurocognitive functions. Neurochemistry International 2009, 55:606-609.
77. Schrijver N.C.A., Wurbel H. Early social deprivation disrupts attentional, but not affective, shifts in rats. Behavioral Neuroscience 2001, 115:437-442.
78. Dalley J.D., Theobald D.T., Pereira E.P., Li P.L., Robbins T.R. Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology 2002, 164:329-340.
79. McLean S.L., Grayson B., Harris M., Protheroe C., Bate S., Woolley M.L., et al. Isolation rearing impairs novel object recognition and attentional set shifting performance in female rats. Journal of Psychopharmacology 2010, 24:57-63.
80. Enomoto T., Floresco S.B. Disruptions in spatial working memory, but not short-term memory, induced by repeated ketamine exposure. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009, 33:668-675.
81. Enomoto T., Noda Y., Nabeshima T. Phencyclidine and genetic animal models of schizophrenia developed in relation to the glutamate hypothesis. Methods and Findings in Experimental and Clinical Pharmacology 2007, 29:291-301.
82. Chatterjee M., Ganguly S., Srivastava M., Palit G. Effect of chronic versus acute ketamine administration and its withdrawal effect on behavioural alterations in mice: implications for experimental psychosis. Behavioural Brain Research 2011, 216:247-254.
83. Winters B.D., Saksida L.M., Bussey T.J. Implications of animal object memory research for human amnesia. Neuropsychologia 2010, 48:2251-2261.
84. Ennaceur A. One-trial object recognition in rats and mice: methodological and theoretical issues. Behavioural Brain Research 2010, 215:244-254.
85. Lyon L., Saksida L.M., Bussey T.J. Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models. Psychopharmacology 2012, 220:647-672.
86. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. Journal of Neuroscience 2005, 25:4243-4251.
87. Winters B.D., Reid J.M. A distributed cortical representation underlies crossmodal object recognition in rats. Journal of Neuroscience 2010, 30:6253-6261.
88. Bianchi M., Fone K.F.C., Azmi N., Heidbreder C.A., Hagan J.J., Marsden C.A. Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. European Journal of Neuroscience 2006, 24:2894-2902.
89. Lapiz M.D., Mateo Y., Parker T., Marsden C. Effects of noradrenaline depletion in the brain on response to novelty in isolation-reared rats. Psychopharmacology 2000, 152:312-320.
90. Robbins T.W., Jones G.H., Wilkinson L.S. Behavioural and neurochemical effects of early social deprivation in the rat. Journal of Psychopharmacology 1996, 10:39-47.
91. Hashimoto K., Fujita Y., Iyo M. Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of fluvoxamine: role of sigma-I receptors. Neuropsychopharmacology 2007, 32:514-521.
92. Hashimoto K., Fujita Y., Shimizu E., Iyo M. Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of clozapine, but not haloperidol. European Journal of Pharmacology 2005, 519:114-117.
93. Tandon R., Nasrallah H.A., Keshavan M.S. Schizophrenia, just the facts 4. Clinical features and conceptualization. Schizophrenia Research 2009, 110:1-23.
94. Berle J., Hauge E., Oedegaard K., Holsten F., Fasmer O. Actigraphic registration of motor activity reveals a more structured behavioural pattern in schizophrenia than in major depression. BMC Research Notes 2010, 3:149.
95. Wirz-Justice A., Haug H.J., Cajochen C. Disturbed circadian rest-activity cycles in schizophrenia patients: an effect of drugs?. Schizophrenia Bulletin 2001, 27:497-502.
96. Farrow T.F.D., Hunter M.D., Wilkinson I.D., Green R.D., Spence S.A. Structural brain correlates of unconstrained motor activity in people with schizophrenia. British Journal of Psychiatry 2005, 187:481-482.
97. Walther S., Koschorke P., Horn H., Strik W. Objectively measured motor activity in schizophrenia challenges the validity of expert ratings. Psychiatry Research 2009, 169:187-190.
98. Walther S., Federspiel A., Horn H., Razavi N., Wiest R., Dierks T., et al. Resting state cerebral blood flow and objective motor activity reveal basal ganglia dysfunction in schizophrenia. Psychiatry Research 2011, 192:117-124.
99. Levine J.B., Leeder A.D., Parekkadan B., Berdichevsky Y., Rauch S.L., Smoller J.W., et al. Isolation rearing impairs wound healing and is associated with increased locomotion and decreased immediate early gene expression in the medial prefrontal cortex of juvenile rats. Neuroscience 2008, 151:589-603.
100. Ferdman N., Murmu R.P., Bock J., Braun K., Leshem M. Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats. Behavioural Brain Research 2007, 180:174-182.
101. Paulus M.P., Varty G.B., Geyer M.A. The genetic liability to stress and postweaning isolation have a competitive influence on behavioral organization in rats. Physiology and Behavior 2000, 68:389-394.
102. Gentsch C., Lichtsteiner M., Frischknecht H.R., Feer H., Siegfried B. Isolation-induced locomotor hyperactivity and hypoalgesia in rats are prevented by handling and reversed by resocialization. Physiology and Behavior 1988, 43:13-16.
103. Bakshi V.P., Geyer M.A. Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats. Physiology and Behavior 1999, 67:385-392.
104. Meng Q., Li N., Han X., Shao F., Wang W. Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neuroscience Letters 2010, 480:25-29.
105. Farber N.B., Wozniak D.F., Price M.T., Labruyere J., Huss J., St.Peter H. Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia?. Biological Psychiatry 1995, 38:788-796.
106. Simpson S.M., Menard J.L., Reynolds J.N., Beninger R.J. Post-weaning social isolation increases activity in a novel environment but decreases defensive burying and subchronic MK-801 enhances the activity but not the burying effect in rats. Pharmacology Biochemistry and Behavior 2010, 95:72-79.
107. Gandal M.J., Anderson R.L., Billingslea E.N., Carlson G.C., Roberts T.P.L., Siegel S.J. Mice with reduced NMDA receptor expression: more consistent with autism than schizophrenia?. Genes, Brain and Behavior 2012, 11:740-750.
108. Hart P.C., Bergner C.L., Smolinsky A.N., Dufour B.D., Egan R.J., LaPorte J.L., et al. Experimental models of anxiety for drug discovery and brain research. Methods in Molecular Biology 2010, 602:299-321.
109. Audet M.C., Goulet S., Dore F.Y. Repeated subchronic exposure to phencyclidine elicits excessive atypical grooming in rats. Behavioural Brain Research 2006, 167:103-110.
110. Clark B.J., Hines D.J., Hamilton D.A., Whishaw I.Q. Movements of exploration intact in rats with hippocampal lesions. Behavioural Brain Research 2005, 163:91-99.
111. Jochum T., Letzsch A., Greiner W., Wagner G., Sauer H., Bar K.J. Influence of antipsychotic medication on pain perception in schizophrenia. Psychiatry Research 2006, 142:151-156.
112. Dworkin R.H. Pain insensitivity in schizophrenia: a neglected phenomenon and some implications. Schizophrenia Bulletin 1994, 20:235-248.
113. Tuboly G., Horvath G. Pain sensitivity changes in patients and animal models. Part I. Ideggyogyaszati Szemle-Clinical Neuroscience 2009, 62:4-11.
114. Van den Berg C.L., Van Ree J.M., Spruijt B.M., Kitchen I. Effects of juvenile isolation and morphine treatment on social interactions and opioid receptors in adult rats: behavioural and autoradiographic studies. European Journal of Neuroscience 1999, 11:3023-3032.
115. Szikszay M., Benedek G. Tolerance to morphine induced by chronic mild environmental stressors. Acta Physiologica Hungarica 1989, 73:447-453.
116. DeFeudis F.V., Defeudis P.A., Somoza E. Altered analgesic responses to morphine in differentially housed mice. Psychopharmacology 1976, 49:117-118.
117. Tuboly G., Horvath G. Pain sensitivity changes in schizophrenic patients and animal models, Part II. Ideggyogyaszati Szemle-Clinical Neuroscience 2009, 62:148-153.
118. Coid J., Yang M. The distribution of psychopathy among a household population: categorical or dimensional?. Social Psychiatry and Psychiatric Epidemiology 2008, 43:773-781.
119. Tryon RC. The genetics of learning ability in rats - a preliminary report. University of California Publications in Psychology 1929;4:71-85.
120. Viggiano D., Vallone D., Welzl H., Sadile A.G. The Naples high- and low-excitability rats: selective breeding, behavioral profile, morphometry, and molecular biology of the mesocortical dopamine system. Behavior Genetics 2002, 32:315-333.
121. Toulopoulou T., Goldberg T.E., Mesa I.R., Picchioni M., Rijsdijk F., Stahl D., et al. Impaired intellect and memory: a missing link between genetic risk and schizophrenia?. Archives of General Psychiatry 2010, 67:905-913.