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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Neurobehavioral Profiles of Six Genetically-based Rat Models of Schizophrenia- related Symptoms

Author(s): Ignasi Oliveras*, Toni Cañete, Daniel Sampedro-Viana, Cristóbal Río-Álamos, Adolf Tobeña, Maria Giuseppa Corda, Osvaldo Giorgi and Alberto Fernández-Teruel*

Volume 21, Issue 9, 2023

Published on: 24 February, 2023

Page: [1934 - 1952] Pages: 19

DOI: 10.2174/1570159X21666230221093644

Price: $65

Abstract

Schizophrenia is a chronic and severe mental disorder with high heterogeneity in its symptoms clusters. The effectiveness of drug treatments for the disorder is far from satisfactory. It is widely accepted that research with valid animal models is essential if we aim at understanding its genetic/ neurobiological mechanisms and finding more effective treatments. The present article presents an overview of six genetically-based (selectively-bred) rat models/strains, which exhibit neurobehavioral schizophrenia-relevant features, i.e., the Apomorphine-susceptible (APO-SUS) rats, the Low-prepulse inhibition rats, the Brattleboro (BRAT) rats, the Spontaneously Hypertensive rats (SHR), the Wisket rats and the Roman High-Avoidance (RHA) rats. Strikingly, all the strains display impairments in prepulse inhibition of the startle response (PPI), which remarkably, in most cases are associated with novelty-induced hyperlocomotion, deficits of social behavior, impairment of latent inhibition and cognitive flexibility, or signs of impaired prefrontal cortex (PFC) function. However, only three of the strains share PPI deficits and dopaminergic (DAergic) psychostimulant-induced hyperlocomotion (together with prefrontal cortex dysfunction in two models, the APO-SUS and RHA), which points out that alterations of the mesolimbic DAergic circuit are a schizophrenia-linked trait that not all models reproduce, but it characterizes some strains that can be valid models of schizophrenia-relevant features and drug-addiction vulnerability (and thus, dual diagnosis). We conclude by putting the research based on these genetically-selected rat models in the context of the Research Domain Criteria (RDoC) framework, suggesting that RDoC-oriented research programs using selectively-bred strains might help to accelerate progress in the various aspects of the schizophrenia-related research agenda.

Graphical Abstract

[1]
Sawa, A.; Snyder, S.H. Schizophrenia: Diverse approaches to a complex disease. Science, 2002, 296(5568), 692-695.
[http://dx.doi.org/10.1126/science.1070532] [PMID: 11976442]
[2]
Powell, C.M.; Miyakawa, T. Schizophrenia-relevant behavioral testing in rodent models: A uniquely human disorder? Biol. Psychiatry, 2006, 59(12), 1198-1207.
[http://dx.doi.org/10.1016/j.biopsych.2006.05.008] [PMID: 16797265]
[3]
Jones, C.A.; Watson, D.J.G.; Fone, K.C.F. Animal models of schizophrenia. Br. J. Pharmacol., 2011, 164(4), 1162-1194.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01386.x] [PMID: 21449915]
[4]
Kapur, S. Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. Am. J. Psychiatry, 2003, 160(1), 13-23.
[http://dx.doi.org/10.1176/appi.ajp.160.1.13] [PMID: 12505794]
[5]
González-Maeso, J.; Ang, R.L.; Yuen, T.; Chan, P.; Weisstaub, N.V.; López-Giménez, J.F.; Zhou, M.; Okawa, Y.; Callado, L.F.; Milligan, G.; Gingrich, J.A.; Filizola, M.; Meana, J.J.; Sealfon, S.C. Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature, 2008, 452(7183), 93-97.
[http://dx.doi.org/10.1038/nature06612] [PMID: 18297054]
[6]
Snyder, S.H. A complex in psychosis. Nature, 2008, 452(7183), 38-39.
[http://dx.doi.org/10.1038/452038a] [PMID: 18322519]
[7]
González-Maeso, J.; Sealfon, S.C. Psychedelics and schizophrenia. Trends Neurosci., 2009, 32(4), 225-232.
[http://dx.doi.org/10.1016/j.tins.2008.12.005] [PMID: 19269047]
[8]
Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature, 2014, 511(7510), 421-427.
[http://dx.doi.org/10.1038/nature13595] [PMID: 25056061]
[9]
Flint, J.; Munafò, M. Genesis of a complex disease. Nature, 2014, 511(7510), 412-413.
[http://dx.doi.org/10.1038/nature13645] [PMID: 25056056]
[10]
Geyer, M.A.; Olivier, B.; Joëls, M.; Kahn, R.S. From antipsychotic to anti-schizophrenia drugs: Role of animal models. Trends Pharmacol. Sci., 2012, 33(10), 515-521.
[http://dx.doi.org/10.1016/j.tips.2012.06.006] [PMID: 22810174]
[11]
Ellenbroek, B.A.; Karl, T. Modeling the psychopathological dimensions of schizophrenia - from molecules to behavior. In: Handbook of Behavioral Neuroscience; Elsevier: Amsterdam, 2016; pp. 303-324.
[http://dx.doi.org/10.1016/B978-0-12-800981-9.00018-3]
[12]
Fernando, A.B.P.; Robbins, T.W. Animal models of neuropsychiatric disorders. Annu. Rev. Clin. Psychol., 2011, 7(1), 39-61.
[http://dx.doi.org/10.1146/annurev-clinpsy-032210-104454] [PMID: 21219191]
[13]
Hayward, A.; Tomlinson, A.; Neill, J.C. Low attentive and high impulsive rats: A translational animal model of ADHD and disorders of attention and impulse control. Pharmacol. Ther., 2016, 158, 41-51.
[http://dx.doi.org/10.1016/j.pharmthera.2015.11.010] [PMID: 26617216]
[14]
Powell, S.B.; Weber, M.; Geyer, M. Genetic models of sensorimotor gating: Relevance to neuropsychiatric disorders. In: Behavioral Neurogenetics. Current Topics in Behavioral Neurosciences; Cryan, J.; Reif, A., Eds.; Springer: Berlin, Heidelberg, 2012; Vol. 12, .
[http://dx.doi.org/10.1007/7854_2011_195]
[15]
Ayhan, Y.; McFarland, R.; Pletnikov, M.V. Animal models of gene–environment interaction in schizophrenia: A dimensional perspective. Prog. Neurobiol., 2016, 136, 1-27.
[http://dx.doi.org/10.1016/j.pneurobio.2015.10.002] [PMID: 26510407]
[16]
Dalley, J.W.; Robbins, T.W. Fractionating impulsivity: Neuropsychiatric implications. Nat. Rev. Neurosci., 2017, 18(3), 158-171.
[http://dx.doi.org/10.1038/nrn.2017.8] [PMID: 28209979]
[17]
Jupp, B.; Caprioli, D.; Dalley, J.W. Highly impulsive rats: Modelling an endophenotype to determine the neurobiological, genetic and environmental mechanisms of addiction. Dis. Model. Mech., 2013, 6(2), dmm.010934.
[http://dx.doi.org/10.1242/dmm.010934] [PMID: 23355644]
[18]
Robinson, E.S.J.; Eagle, D.M.; Economidou, D.; Theobald, D.E.H.; Mar, A.C.; Murphy, E.R.; Robbins, T.W.; Dalley, J.W. Behavioural characterisation of high impulsivity on the 5-choice serial reaction time task: Specific deficits in ‘waiting’ versus ‘stopping’. Behav. Brain Res., 2009, 196(2), 310-316.
[http://dx.doi.org/10.1016/j.bbr.2008.09.021] [PMID: 18940201]
[19]
Merchán, A.; Mora, S.; Gago, B.; Rodriguez-Ortega, E.; Fernández-Teruel, A.; Puga, J.L.; Sánchez-Santed, F.; Moreno, M.; Flores, P. Excessive habit formation in schedule-induced polydipsia: Microstructural analysis of licking among rat strains and involvement of the orbitofrontal cortex. Genes Brain Behav., 2019, 18(3), e12489.
[http://dx.doi.org/10.1111/gbb.12489] [PMID: 29877027]
[20]
Oliveras, I.; Río-Álamos, C.; Cañete, T.; Blázquez, G.; Martínez-Membrives, E.; Giorgi, O.; Corda, M.G.; Tobeña, A.; Fernández-Teruel, A. Prepulse inhibition predicts spatial working memory performance in the inbred Roman high- and low-avoidance rats and in genetically heterogeneous NIH-HS rats: Relevance for studying pre-attentive and cognitive anomalies in schizophrenia. Front. Behav. Neurosci., 2015, 9, 213.
[http://dx.doi.org/10.3389/fnbeh.2015.00213] [PMID: 26347624]
[21]
Østerbøg, T.B.; On, D.M.; Oliveras, I.; Río-Álamos, C.; Sanchez-Gonzalez, A.; Tapias-Espinosa, C.; Tobeña, A.; González-Maeso, J.; Fernández-Teruel, A.; Aznar, S. Metabotropic glutamate receptor 2 and dopamine receptor 2 gene expression predict sensorimotor gating response in the genetically heterogeneous NIH-HS rat strain. Mol. Neurobiol., 2020, 57(3), 1516-1528.
[http://dx.doi.org/10.1007/s12035-019-01829-w] [PMID: 31782106]
[22]
Tapias-Espinosa, C.; Río-Álamos, C.; Sánchez-González, A.; Oliveras, I.; Sampedro-Viana, D.; Castillo-Ruiz, M.M.; Cañete, T.; Tobeña, A.; Fernández-Teruel, A. Schizophrenia-like reduced sensorimotor gating in intact inbred and outbred rats is associated with decreased medial prefrontal cortex activity and volume. Neuropsychopharmacology, 2019, 44(11), 1975-1984.
[http://dx.doi.org/10.1038/s41386-019-0392-x] [PMID: 30986819]
[23]
Cools, A.R.; Brachten, R.; Heeren, D.; Willemen, A.; Ellenbroek, B. Search after neurobiological profile of individual-specific features of wistar rats. Brain Res. Bull., 1990, 24(1), 49-69.
[http://dx.doi.org/10.1016/0361-9230(90)90288-B] [PMID: 2310946]
[24]
Ellenbroek, B.A.; Geyer, M.A.; Cools, A.R. The behavior of APO-SUS rats in animal models with construct validity for schizophrenia. J. Neurosci., 1995, 15(11), 7604-7611.
[http://dx.doi.org/10.1523/JNEUROSCI.15-11-07604.1995] [PMID: 7472511]
[25]
Ellenbroek, B.A.; Cools, A.R. Apomorphine susceptibility and animal models for psychopathology: Genes and environment. Behav. Genet., 2002, 32(5), 349-361.
[http://dx.doi.org/10.1023/A:1020214322065] [PMID: 12405516]
[26]
Rots, N.Y.; Cools, A.R.; Bérod, A.; Voorn, P.; Rostène, W.; de Kloet, E.R. Rats bred for enhanced apomorphine susceptibility have elevated tyrosine hydroxylase mRNA and dopamine D2-receptor binding sites in nigrostriatal and tuberoinfundibular dopamine systems. Brain Res., 1996, 710(1-2), 189-196.
[http://dx.doi.org/10.1016/0006-8993(95)01379-2] [PMID: 8963658]
[27]
Cools, A.R.; Ellenbroek, B.A.; Gingras, M.A.; Engbersen, A.; Heeren, D. Differences in vulnerability and susceptibility to dexamphetamine in Nijmegen high and low responders to novelty: A dose-effect analysis of spatio-temporal programming of behaviour. Psychopharmacology (Berl.), 1997, 132(2), 181-187.
[http://dx.doi.org/10.1007/s002130050334] [PMID: 9266615]
[28]
Gingras, M.A.; Cools, A.R. No major differences in locomotor responses to dexamphetamine in high and low responders to novelty: A study in Wistar rats. Pharmacol. Biochem. Behav., 1997, 57(4), 857-862.
[http://dx.doi.org/10.1016/S0091-3057(96)00320-6] [PMID: 9259016]
[29]
Gingras, M.A.; Cools, A.R. Different behavioral effects of daily or intermittent dexamphetamine administration in Nijmegen high and low responders. Psychopharmacology (Berl.), 1997, 132(2), 188-194.
[http://dx.doi.org/10.1007/s002130050335] [PMID: 9266616]
[30]
van der Elst, M.C.J.; Ellenbroek, B.A.; Cools, A.R. Cocaine strongly reduces prepulse inhibition in apomorphine-susceptible rats, but not in apomorphine-unsusceptible rats: Regulation by dopamine D2 receptors. Behav. Brain Res., 2006, 175(2), 392-398.
[http://dx.doi.org/10.1016/j.bbr.2006.09.014] [PMID: 17079027]
[31]
Maas, D.A.; Eijsink, V.D.; Spoelder, M.; van Hulten, J.A.; De Weerd, P.; Homberg, J.R.; Vallès, A.; Nait-Oumesmar, B.; Martens, G.J.M. Interneuron hypomyelination is associated with cognitive inflexibility in a rat model of schizophrenia. Nat. Commun., 2020, 11(1), 2329.
[http://dx.doi.org/10.1038/s41467-020-16218-4] [PMID: 32393757]
[32]
Maas, D.A.; Eijsink, V.D.; van Hulten, J.A.; Panic, R.; De Weerd, P.; Homberg, J.R.; Vallès, A.; Nait-Oumesmar, B.; Martens, G.J.M. Antioxidant treatment ameliorates prefrontal hypomyelination and cognitive deficits in a rat model of schizophrenia. Neuropsychopharmacology, 2021, 46(6), 1161-1171.
[http://dx.doi.org/10.1038/s41386-021-00964-0] [PMID: 33564104]
[33]
Ellenbroek, B.A.; Sluyter, F.; Cools, A.R. The role of genetic and early environmental factors in determining apomorphine susceptibility. Psychopharmacology (Berl.), 2000, 148(2), 124-131.
[http://dx.doi.org/10.1007/s002130050033] [PMID: 10663426]
[34]
van Os, J.; Kenis, G.; Rutten, B.P.F. The environment and schizophrenia. Nature, 2010, 468(7321), 203-212.
[http://dx.doi.org/10.1038/nature09563] [PMID: 21068828]
[35]
Cabib, S.; Oliverio, A.; Ventura, R.; Lucchese, F.; Puglisi-Allegra, S. Brain dopamine receptor plasticity: Testing a diathesis-stress hypothesis in an animal model. Psychopharmacology (Berl.), 1997, 132(2), 153-160.
[http://dx.doi.org/10.1007/s002130050331] [PMID: 9266612]
[36]
Birkett, S.D.; Pickering, B.T. The vasopressin precursor in the Brattleboro (di/di) rat. Int. J. Pept. Protein Res., 1988, 32(6), 565-572.
[http://dx.doi.org/10.1111/j.1399-3011.1988.tb01388.x] [PMID: 3246481]
[37]
Bouby, N.; Hassler, C.; Bankir, L. Contribution of vasopressin to progression of chronic renal failure: Study in Brattleboro rats. Life Sci., 1999, 65(10), 991-1004.
[http://dx.doi.org/10.1016/S0024-3205(99)00330-6] [PMID: 10499867]
[38]
Valtin, H.; Schroeder, H.A. Familial hypothalamic diabetes insipidus in rats (Brattleboro strain). Am. J. Physiol., 1964, 206(2), 425-430.
[http://dx.doi.org/10.1152/ajplegacy.1964.206.2.425] [PMID: 14120453]
[39]
Berquist, M.D., II; Mooney-Leber, S.M.; Feifel, D.; Prus, A.J. Assessment of attention in male and female Brattleboro rats using a self-paced five-choice serial reaction time task. Brain Res., 2013, 1537, 174-179.
[http://dx.doi.org/10.1016/j.brainres.2013.09.012] [PMID: 24055104]
[40]
Cilia, J.; Gartlon, J.E.; Shilliam, C.; Dawson, L.A.; Moore, S.H.; Jones, D.N.C. Further neurochemical and behavioural investigation of Brattleboro rats as a putative model of schizophrenia. J. Psychopharmacol., 2010, 24(3), 407-419.
[http://dx.doi.org/10.1177/0269881108098787] [PMID: 19204063]
[41]
Feifel, D.; Priebe, K. Vasopressin-deficient rats exhibit sensorimotor gating deficits that are reversed by subchronic haloperidol. Biol. Psychiatry, 2001, 50(6), 425-433.
[http://dx.doi.org/10.1016/S0006-3223(01)01100-3] [PMID: 11566159]
[42]
Feifel, D.; Priebe, K. The effects of cross-fostering on inherent sensorimotor gating deficits exhibited by Brattleboro rats. J. Gen. Psychol., 2007, 134(2), 173-182.
[http://dx.doi.org/10.3200/GENP.134.2.172-182] [PMID: 17503693]
[43]
Feifel, D.; Mexal, S.; Melendez, G.; Liu, P.Y.T.; Goldenberg, J.R.; Shilling, P.D. The brattleboro rat displays a natural deficit in social discrimination that is restored by clozapine and a neurotensin analog. Neuropsychopharmacology, 2009, 34(8), 2011-2018.
[http://dx.doi.org/10.1038/npp.2009.15] [PMID: 19322170]
[44]
Feifel, D.; Shilling, P.D.; Melendez, G. Further characterization of the predictive validity of the Brattleboro rat model for antipsychotic efficacy. J. Psychopharmacol., 2011, 25(6), 836-841.
[http://dx.doi.org/10.1177/0269881110388327] [PMID: 21106605]
[45]
Török, B.; Fodor, A.; Klausz, B.; Varga, J.; Zelena, D. Ameliorating schizophrenia-like symptoms in vasopressin deficient male Brattleboro rat by chronic antipsychotic treatment. Eur. J. Pharmacol., 2021, 909, 174383.
[http://dx.doi.org/10.1016/j.ejphar.2021.174383] [PMID: 34332923]
[46]
De Wied, D.; Joëls, M.; Burbach, J.P.H.; De Jong, W.; De Kloet, E.R.; Gaffori, O.W.J.; Urban, I.J.A.; Van Ree, J.M.; Van Wimersma Greidanus, T.B.; Veldhuis, H.D.; Versteeg, D.H.G.; Wiegant, V.M. Vasopressin effects on the central nervous system. In: Peptide hormones: Effects and mechanisms of action; Negro-Vilar, A.; Conn, P.M., Eds.; CRC Press: Florida, USA, 1988; Vol. I, pp. 97-140.
[47]
Aarde, S.M.; Jentsch, J.D. Haploinsufficiency of the arginine–vasopressin gene is associated with poor spatial working memory performance in rats. Horm. Behav., 2006, 49(4), 501-508.
[http://dx.doi.org/10.1016/j.yhbeh.2005.11.002] [PMID: 16375903]
[48]
Colombo, G.; Hansen, C.; Hoffman, P.L.; Grant, K.A. Decreased performance in a delayed alternation task by rats genetically deficient in vasopressin. Physiol. Behav., 1992, 52(4), 827-830.
[http://dx.doi.org/10.1016/0031-9384(92)90422-X] [PMID: 1409961]
[49]
Varga, J.; Klausz, B.; Domokos, Á.; Kálmán, S.; Pákáski, M. Szűcs, S.; Garab, D.; Zvara, Á.; Puskás, L.; Kálmán, J.; Tímár, J.; Bagdy, G.; Zelena, D. Increase in Alzheimer’s related markers preceeds memory disturbances: Studies in vasopressin-deficient Brattleboro rat. Brain Res. Bull., 2014, 100, 6-13.
[http://dx.doi.org/10.1016/j.brainresbull.2013.10.010] [PMID: 24177174]
[50]
Lin, R.E.; Ambler, L.; Billingslea, E.N.; Suh, J.; Batheja, S.; Tatard-Leitman, V.; Featherstone, R.E.; Siegel, S.J. Electroencephalographic and early communicative abnormalities in Brattleboro rats. Physiol. Rep., 2013, 1(5), e00100.
[http://dx.doi.org/10.1002/phy2.100] [PMID: 24303172]
[51]
Dawson, R., Jr; Wallace, D.R.; King, M.J. Monoamine and amino acid content in brain regions of Brattleboro rats. Neurochem. Res., 1990, 15(7), 755-761.
[http://dx.doi.org/10.1007/BF00973658] [PMID: 1697655]
[52]
Feenstra, M.G.P.; Snijdewint, F.G.M.; Van Galen, H.; Boer, G.J. Widespread alterations in central noradrenaline, dopamine, and serotonin systems in the Brattleboro rat not related to the local absence of vasopressin. Neurochem. Res., 1990, 15(3), 283-288.
[http://dx.doi.org/10.1007/BF00968673] [PMID: 1694974]
[53]
Shilling, P.D.; Kinkead, B.; Murray, T.; Melendez, G.; Nemeroff, C.B.; Feifel, D. Upregulation of striatal dopamine-2 receptors in Brattleboro rats with prepulse inhibition deficits. Biol. Psychiatry, 2006, 60(11), 1278-1281.
[http://dx.doi.org/10.1016/j.biopsych.2006.03.045] [PMID: 16814260]
[54]
Brito, G.N.O.; Thomas, G.J.; Gash, D.M.; Kitchen, J.H. The behavior of Brattleboro rats. Ann. N. Y. Acad. Sci., 1982, 394(1 The Brattlebo), 740-748.
[http://dx.doi.org/10.1111/j.1749-6632.1982.tb37492.x] [PMID: 6960792]
[55]
Laycock, J.F.; Gartside, I.B.; Chapman, J.T. A comparison of the learning abilities of Brattleboro rats with hereditary diabetes insipidus and Long-Evans rats using positively reinforced operant conditioning. Prog. Brain Res., 1983, 60, 183-187.
[http://dx.doi.org/10.1016/S0079-6123(08)64385-X] [PMID: 6665137]
[56]
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(3), 612-622.
[http://dx.doi.org/10.1016/j.neuroscience.2007.06.034] [PMID: 17693035]
[57]
Schwabe, K.; Freudenberg, F.; Koch, M. Selective breeding of reduced sensorimotor gating in Wistar rats. Behav. Genet., 2007, 37(5), 706-712.
[http://dx.doi.org/10.1007/s10519-007-9166-z] [PMID: 17899353]
[58]
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. Behav. Brain Res., 2007, 177(2), 364-367.
[http://dx.doi.org/10.1016/j.bbr.2006.11.037] [PMID: 17182114]
[59]
Lysaker, P.H.; Bell, M.D.; Bryson, G.; Kaplan, E. Neurocognitive function and insight in schizophrenia: Support for an association with impairments in executive function but not with impairments in global function. Acta Psychiatr. Scand., 1998, 97(4), 297-301.
[http://dx.doi.org/10.1111/j.1600-0447.1998.tb10003.x] [PMID: 9570491]
[60]
Perry, W.; Braff, D.L. A multimethod approach to assessing perseverations in schizophrenia patients. Schizophr. Res., 1998, 33(1-2), 69-77.
[http://dx.doi.org/10.1016/S0920-9964(98)00061-9] [PMID: 9783346]
[61]
Dieckmann, M.; Freudenberg, F.; Klein, S.; Koch, M.; Schwabe, K. Disturbed social behavior and motivation in rats selectively bred for deficient sensorimotor gating. Schizophr. Res., 2007, 97(1-3), 250-253.
[http://dx.doi.org/10.1016/j.schres.2007.08.007] [PMID: 17855056]
[62]
Rhein, M.; Muschler, M.R.; Krauss, J.K.; Bleich, S.; Frieling, H.; Schwabe, K. Hypomethylation of neuregulin in rats selectively bred for reduced sensorimotor gating. Schizophr. Res., 2013, 150(1), 262-265.
[http://dx.doi.org/10.1016/j.schres.2013.07.012] [PMID: 23899995]
[63]
Weickert, C.S.; Tiwari, Y.; Schofield, P.R.; Mowry, B.J.; Fullerton, J.M. Schizophrenia-associated HapICE haplotype is associated with increased NRG1 type III expression and high nucleotide diversity. Transl. Psychiatry, 2012, 2(4), e104.
[http://dx.doi.org/10.1038/tp.2012.25] [PMID: 22832904]
[64]
Alam, M.; Angelov, S.; Stemmler, M.; von Wrangel, C.; Krauss, J.K.; Schwabe, K. Neuronal activity of the prefrontal cortex is reduced in rats selectively bred for deficient sensorimotor gating. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2015, 56, 174-184.
[http://dx.doi.org/10.1016/j.pnpbp.2014.08.017] [PMID: 25220677]
[65]
Brisch, R.; Saniotis, A.; Wolf, R.; Bielau, H.; Bernstein, H.G.; Steiner, J.; Bogerts, B.; Braun, A.K.; Jankowski, Z.; Kumaritlake, J.; Henneberg, M.; Gos, T. The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: Old fashioned, but still in vogue. Front. Psychiatry, 2014, 5, 47.
[http://dx.doi.org/10.3389/fpsyt.2014.00047] [PMID: 24904434]
[66]
Giorgi, O.; Piras, G.; Corda, M.G. The psychogenetically selected Roman high- and low-avoidance rat lines: A model to study the individual vulnerability to drug addiction. Neurosci. Biobehav. Rev., 2007, 31(1), 148-163.
[http://dx.doi.org/10.1016/j.neubiorev.2006.07.008] [PMID: 17164110]
[67]
Giorgi, O.; Corda, M.G.; Fernández-Teruel, A. A genetic model of impulsivity, vulnerability to drug abuse and schizophrenia-relevant symptoms with translational potential: The roman high- vs. low-avoidance rats. Front. Behav. Neurosci., 2019, 13, 145.
[http://dx.doi.org/10.3389/fnbeh.2019.00145] [PMID: 31333426]
[68]
Braff, D.L.; Geyer, M.A.; Swerdlow, N.R. Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl.), 2001, 156(2-3), 234-258.
[http://dx.doi.org/10.1007/s002130100810] [PMID: 11549226]
[69]
Swerdlow, N.R.; Martinez, Z.A.; Hanlon, F.M.; Platten, A.; Farid, M.; Auerbach, P.; Braff, D.L.; Geyer, M.A. Toward understanding the biology of a complex phenotype: Rat strain and substrain differences in the sensorimotor gating-disruptive effects of dopamine agonists. J. Neurosci., 2000, 20(11), 4325-4336.
[http://dx.doi.org/10.1523/JNEUROSCI.20-11-04325.2000] [PMID: 10818168]
[70]
Swerdlow, N.R.; Shoemaker, J.M.; Platten, A.; Pitcher, L.; Goins, J.; Auerbach, P.P. Heritable differences in the dopaminergic regulation of sensorimotor gating. Psychopharmacology (Berl.), 2004, 174(4), 441-451.
[http://dx.doi.org/10.1007/s00213-003-1481-3] [PMID: 15300358]
[71]
Swerdlow, N.R.; Shilling, P.D.; Breier, M.; Trim, R.S.; Light, G.A.; Marie, R.S. Fronto-temporal-mesolimbic gene expression and heritable differences in amphetamine-disrupted sensorimotor gating in rats. Psychopharmacology (Berl.), 2012, 224(3), 349-362.
[http://dx.doi.org/10.1007/s00213-012-2758-1] [PMID: 22700037]
[72]
John, N.; Theilmann, W.; Frieling, H.; Krauss, J.K.; Alam, M.; Schwabe, K.; Brandt, C. Cortical electroconvulsive stimulation alleviates breeding-induced prepulse inhibition deficit in rats. Exp. Neurol., 2016, 275(Pt 1), 99-103.
[http://dx.doi.org/10.1016/j.expneurol.2015.10.003] [PMID: 26476178]
[73]
Angelov, S.D.; Dietrich, C.; Krauss, J.K.; Schwabe, K. Effect of deep brain stimulation in rats selectively bred for reduced prepulse inhibition. Brain Stimul., 2014, 7(4), 595-602.
[http://dx.doi.org/10.1016/j.brs.2014.03.013] [PMID: 24794286]
[74]
Horvath, G.; Liszli, P.; Kekesi, G.; Büki, A.; Benedek, G. Characterization of exploratory activity and learning ability of healthy and “schizophrenia-like” rats in a square corridor system (AMBITUS). Physiol. Behav., 2017, 169, 155-164.
[http://dx.doi.org/10.1016/j.physbeh.2016.11.039] [PMID: 27923717]
[75]
Horvath, G.; Petrovszki, Z.; Kekesi, G.; Tuboly, G.; Bodosi, B.; Horvath, J. Gombkötő P.; Benedek, G.; Nagy, A. Electrophysiological alterations in a complex rat model of schizophrenia. Behav. Brain Res., 2016, 307, 65-72.
[http://dx.doi.org/10.1016/j.bbr.2016.03.051] [PMID: 27036646]
[76]
Kekesi, G.; Petrovszki, Z.; Benedek, G.; Horvath, G. Sex-specific alterations in behavioral and cognitive functions in a “three hit” animal model of schizophrenia. Behav. Brain Res., 2015, 284, 85-93.
[http://dx.doi.org/10.1016/j.bbr.2015.02.015] [PMID: 25698594]
[77]
Petrovszki, Z.; Adam, G.; Tuboly, G.; Kekesi, G.; Benedek, G.; Keri, S.; Horvath, G. Characterization of gene–environment interactions by behavioral profiling of selectively bred rats: The effect of NMDA receptor inhibition and social isolation. Behav. Brain Res., 2013, 240, 134-145.
[http://dx.doi.org/10.1016/j.bbr.2012.11.022] [PMID: 23195116]
[78]
Büki, A.; Horvath, G.; Benedek, G.; Ducza, E.; Kekesi, G. Impaired GAD1 expression in schizophrenia-related WISKET rat model with sex-dependent aggressive behavior and motivational deficit. Genes Brain Behav., 2019, 18(4), e12507.
[http://dx.doi.org/10.1111/gbb.12507] [PMID: 30051606]
[79]
Horvath, G.; Liszli, P.; Kekesi, G.; Büki, A.; Benedek, G. Cognitive training improves the disturbed behavioral architecture of schizophrenia-like rats, “Wisket”. Physiol. Behav., 2019, 201, 70-82.
[http://dx.doi.org/10.1016/j.physbeh.2018.12.011] [PMID: 30576695]
[80]
Büki, A.; Bohár, Z.; Kekesi, G.; Vécsei, L.; Horvath, G. Wisket rat model of schizophrenia: Impaired motivation and, altered brain structure, but no anhedonia. Physiol. Behav., 2022, 244, 113651.
[http://dx.doi.org/10.1016/j.physbeh.2021.113651] [PMID: 34800492]
[81]
Banki, L.; Büki, A.; Horvath, G.; Kekesi, G.; Kis, G.; Somogyvári, F.; Jancsó, G.; Vécsei, L.; Varga, E.; Tuboly, G. Distinct changes in chronic pain sensitivity and oxytocin receptor expression in a new rat model (Wisket) of schizophrenia. Neurosci. Lett., 2020, 714, 134561.
[http://dx.doi.org/10.1016/j.neulet.2019.134561] [PMID: 31629032]
[82]
Uhrig, S.; Hirth, N.; Broccoli, L.; von Wilmsdorff, M.; Bauer, M.; Sommer, C.; Zink, M.; Steiner, J.; Frodl, T.; Malchow, B.; Falkai, P.; Spanagel, R.; Hansson, A.C.; Schmitt, A. Reduced oxytocin receptor gene expression and binding sites in different brain regions in schizophrenia: A post-mortem study. Schizophr. Res., 2016, 177(1-3), 59-66.
[http://dx.doi.org/10.1016/j.schres.2016.04.019] [PMID: 27132494]
[83]
Szűcs, E.; Büki, A.; Kékesi, G.; Horváth, G.; Benyhe, S. Mu-Opioid (MOP) receptor mediated G-protein signaling is impaired in specific brain regions in a rat model of schizophrenia. Neurosci. Lett., 2016, 619, 29-33.
[http://dx.doi.org/10.1016/j.neulet.2016.02.060] [PMID: 26946106]
[84]
Szűcs, E.; Dvorácskó, S.; Tömböly, C.; Büki, A.; Kékesi, G.; Horváth, G.; Benyhe, S. Decreased CB receptor binding and cannabinoid signaling in three brain regions of a rat model of schizophrenia. Neurosci. Lett., 2016, 633, 87-93.
[http://dx.doi.org/10.1016/j.neulet.2016.09.020] [PMID: 27639959]
[85]
Szűcs, E.; Ducza, E.; Büki, A.; Kekesi, G.; Benyhe, S.; Horvath, G. Characterization of dopamine D2 receptor binding, expression and signaling in different brain regions of control and schizophrenia-model Wisket rats. Brain Res., 2020, 1748, 147074.
[http://dx.doi.org/10.1016/j.brainres.2020.147074] [PMID: 32858029]
[86]
Okamoto, K.; Aoki, K. Development of a strain of spontaneously hypertensive rats. Jpn. Circ. J., 1963, 27(3), 282-293.
[http://dx.doi.org/10.1253/jcj.27.282] [PMID: 13939773]
[87]
Sagvolden, T.; Metzger, M.A.; Schiørbeck, H.K.; Rugland, A.L.; Spinnangr, I.; Sagvolden, G. The spontaneously hypertensive rat (SHR) as an animal model of childhood hyperactivity (ADHD): Changed reactivity to reinforcers and to psychomotor stimulants. Behav. Neural Biol., 1992, 58(2), 103-112.
[http://dx.doi.org/10.1016/0163-1047(92)90315-U] [PMID: 1360797]
[88]
Levin, R.; Calzavara, M.B.; Santos, C.M.; Medrano, W.A.; Niigaki, S.T.; Abílio, V.C. Spontaneously Hypertensive Rats (SHR) present deficits in prepulse inhibition of startle specifically reverted by clozapine. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2011, 35(7), 1748-1752.
[http://dx.doi.org/10.1016/j.pnpbp.2011.06.003] [PMID: 21693159]
[89]
Calzavara, M.B.; Levin, R.; Medrano, W.A.; Almeida, V.; Sampaio, A.P.F.; Barone, L.C.; Frussa-Filho, R.; Abílio, V.C. Effects of antipsychotics and amphetamine on social behaviors in spontaneously hypertensive rats. Behav. Brain Res., 2011, 225(1), 15-22.
[http://dx.doi.org/10.1016/j.bbr.2011.06.026] [PMID: 21741413]
[90]
Calzavara, M.B.; Medrano, W.A.; Levin, R.; Kameda, S.R.; Andersen, M.L.; Tufik, S.; Silva, R.H.; Frussa-Filho, R.; Abílio, V.C. Neuroleptic drugs revert the contextual fear conditioning deficit presented by spontaneously hypertensive rats: A potential animal model of emotional context processing in schizophrenia? Schizophr. Bull., 2009, 35(4), 748-759.
[http://dx.doi.org/10.1093/schbul/sbn006] [PMID: 18281713]
[91]
Calzavara, M.B.; Medrano, W.A.; Levin, R.; Libânio, T.C.; de Alencar Ribeiro, R.; Abílio, V.C. The contextual fear conditioning deficit presented by spontaneously hypertensive rats (SHR) is not improved by mood stabilizers. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2011, 35(7), 1607-1611.
[http://dx.doi.org/10.1016/j.pnpbp.2011.06.005] [PMID: 21708209]
[92]
Schaefer, C.F.; Brackett, D.J.; Gunn, C.G.; Wilson, M.F. Behavioral hyperreactivity in the spontaneously hypertensive rat compared to its normotensive progenitor. Pavlov. J. Biol. Sci., 1978, 13(4), 211-216.
[http://dx.doi.org/10.1007/BF03002256] [PMID: 748844]
[93]
Almeida, V.; Peres, F.F.; Levin, R.; Suiama, M.A.; Calzavara, M.B.; Zuardi, A.W.; Hallak, J.E.; Crippa, J.A.; Abílio, V.C. Effects of cannabinoid and vanilloid drugs on positive and negative-like symptoms on an animal model of schizophrenia: The SHR strain. Schizophr. Res., 2014, 153(1-3), 150-159.
[http://dx.doi.org/10.1016/j.schres.2014.01.039] [PMID: 24556469]
[94]
Levin, R.; Peres, F.F.; Almeida, V.; Calzavara, M.B.; Zuardi, A.W.; Hallak, J.E.C.; Crippa, J.A.S.; Abílio, V.C. Effects of cannabinoid drugs on the deficit of prepulse inhibition of startle in an animal model of schizophrenia: The SHR strain. Front. Pharmacol., 2014, 5, 10.
[http://dx.doi.org/10.3389/fphar.2014.00010] [PMID: 24567721]
[95]
Oades, R.D.; Sadile, A.G.; Sagvolden, T.; Viggiano, D.; Zuddas, A.; Devoto, P.; Aase, H.; Johansen, E.B.; Ruocco, L.A.; Russell, V.A. The control of responsiveness in ADHD by catecholamines: Evidence for dopaminergic, noradrenergic and interactive roles. Dev. Sci., 2005, 8(2), 122-131.
[http://dx.doi.org/10.1111/j.1467-7687.2005.00399.x] [PMID: 15720370]
[96]
Li, Q.; Lu, G.; Antonio, G.; Mak, Y.; Rudd, J.; Fan, M.; Yew, D. The usefulness of the spontaneously hypertensive rat to model attention-deficit/hyperactivity disorder (ADHD) may be explained by the differential expression of dopamine-related genes in the brain. Neurochem. Int., 2007, 50(6), 848-857.
[http://dx.doi.org/10.1016/j.neuint.2007.02.005] [PMID: 17395336]
[97]
Russell, V.; de Villiers, A.; Sagvolden, T.; Lamm, M.; Taljaard, J. Altered dopaminergic function in the prefrontal cortex, nucleus accumbens and caudate-putamen of an animal model of attention-deficit hyperactivity disorder — the spontaneously hypertensive rat. Brain Res., 1995, 676(2), 343-351.
[http://dx.doi.org/10.1016/0006-8993(95)00135-D] [PMID: 7614004]
[98]
Kujirai, K.; Przedborski, S.; Kostic, V.; Jackson-Lewis, V.; Fahn, S.; Cadet, J.L. Autoradiography of dopamine receptors and dopamine uptake sites in the spontaneously hypertensive rat. Brain Res. Bull., 1990, 25(5), 703-709.
[http://dx.doi.org/10.1016/0361-9230(90)90046-3] [PMID: 2149666]
[99]
Kirouac, G.J.; Ganguly, P.K. Up-regulation of dopamine receptors in the brain of the spontaneously hypertensive rat: An autoradiographic analysis. Neuroscience, 1993, 52(1), 135-141.
[http://dx.doi.org/10.1016/0306-4522(93)90188-L] [PMID: 8433803]
[100]
Lim, D.K.; Ito, Y.; Hoskins, B.; Rockhold, R.W.; Ho, I.K. Comparative studies of muscarinic and dopamine receptors in three strains of rat. Eur. J. Pharmacol., 1989, 165(2-3), 279-287.
[http://dx.doi.org/10.1016/0014-2999(89)90722-X] [PMID: 2673798]
[101]
Lim, D.K.; Yu, Z.J.; Hoskins, B.; Rockhold, R.W.; Ho, I.K. Effects of acute and subacute cocaine administration on the CNS dopaminergic system in Wistar-Kyoto and spontaneously hypertensive rats: II. Dopamine receptors. Neurochem. Res., 1990, 15(6), 621-627.
[http://dx.doi.org/10.1007/BF00973753] [PMID: 2145522]
[102]
Watanabe, Y.; Fujita, M.; Ito, Y.; Okada, T.; Kusuoka, H.; Nishimura, T. Brain dopamine transporter in spontaneously hypertensive rats. J. Nucl. Med., 1997, 38(3), 470-474.
[PMID: 9074541]
[103]
Van Den Buuse, M.; Richard Jones, C.; Wagner, J. Brain dopamine D-2 receptor mechanisms in spontaneously hypertensive rats. Brain Res. Bull., 1992, 28(2), 289-297.
[http://dx.doi.org/10.1016/0361-9230(92)90190-9] [PMID: 1375862]
[104]
Linthorst, A.C.E.; De Jong, W.; De Boer, T.; Versteeg, D.H.G. Dopamine D1 and D2 receptors in the caudate nucleus of spontaneously hypertensive rats and normotensive Wistar-Kyoto rats. Brain Res., 1993, 602(1), 119-125.
[http://dx.doi.org/10.1016/0006-8993(93)90250-Q] [PMID: 8448648]
[105]
Watanabe, M.; Tsuruta, S.; Inoue, Y.; Kinuya, M.; Ogawa, K.; Mamiya, G.; Tatsunuma, T. Dopamine D1 and D2 receptors in spontaneously hypertensive rat brain striatum. Can. J. Physiol. Pharmacol., 1989, 67(12), 1596-1597.
[http://dx.doi.org/10.1139/y89-256] [PMID: 2697462]
[106]
Bizot, J.C.; Chenault, N.; Houzé, B.; Herpin, A.; David, S.; Pothion, S.; Trovero, F. Methylphenidate reduces impulsive behaviour in juvenile Wistar rats, but not in adult Wistar, SHR and WKY rats. Psychopharmacology (Berl.), 2007, 193(2), 215-223.
[http://dx.doi.org/10.1007/s00213-007-0781-4] [PMID: 17406857]
[107]
van den Bergh, F.S.; Bloemarts, E.; Chan, J.S.W.; Groenink, L.; Olivier, B.; Oosting, R.S. Spontaneously hypertensive rats do not predict symptoms of attention-deficit hyperactivity disorder. Pharmacol. Biochem. Behav., 2006, 83(3), 380-390.
[http://dx.doi.org/10.1016/j.pbb.2006.02.018] [PMID: 16580713]
[108]
Diana, M.C.; Santoro, M.L.; Xavier, G.; Santos, C.M.; Spindola, L.N.; Moretti, P.N.; Ota, V.K.; Bressan, R.A.; Abilio, V.C.; Belangero, S.I. Low expression of Gria1 and Grin1 glutamate receptors in the nucleus accumbens of Spontaneously Hypertensive Rats (SHR). Psychiatry Res., 2015, 229(3), 690-694.
[http://dx.doi.org/10.1016/j.psychres.2015.08.021] [PMID: 26296755]
[109]
Santoro, M.L.; Santos, C.M.; Ota, V.K.; Gadelha, A.; Stilhano, R.S.; Diana, M.C.; Silva, P.N.; Spíndola, L.M.N.; Melaragno, M.I.; Bressan, R.A.; Han, S.W.; Abílio, V.C.; Belangero, S.I. Expression profile of neurotransmitter receptor and regulatory genes in the prefrontal cortex of spontaneously hypertensive rats: Relevance to neuropsychiatric disorders. Psychiatry Res., 2014, 219(3), 674-679.
[http://dx.doi.org/10.1016/j.psychres.2014.05.034] [PMID: 25041985]
[110]
Ferguson, S.A.; Cada, A.M. Spatial learning/memory and social and nonsocial behaviors in the Spontaneously Hypertensive, Wistar–Kyoto and Sprague–Dawley rat strains. Pharmacol. Biochem. Behav., 2004, 77(3), 583-594.
[http://dx.doi.org/10.1016/j.pbb.2003.12.014] [PMID: 15006470]
[111]
Buuse, M. Prepulse inhibition of acoustic startle in spontaneously hypertensive rats. Behav. Brain Res., 2004, 154(2), 331-337.
[http://dx.doi.org/10.1016/j.bbr.2004.02.021] [PMID: 15313020]
[112]
Bignami, G. Selection for high rates and low rates of avoidance conditioning in the rat. Anim. Behav., 1965, 13(2-3), 221-227.
[http://dx.doi.org/10.1016/0003-3472(65)90038-2] [PMID: 5835838]
[113]
Driscoll, P.; Bättig, K. Behavioural, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance. In: Genetics of the Brain; Lieblich, I., Ed.; Elsevier: Amsterdam, 1982; pp. 95-123.
[114]
Driscoll, P.; Escorihuela, R.M.; Fernández-Teruel, A.; Giorgi, O.; Schwegler, H.; Steimer, T.; Wiersma, A.; Corda, M.G.; Flint, J.; Koolhaas, J.M.; Langhans, W.; Schulz, P.E.; Siegel, J.; Tobeña, A. Genetic selection and differential stress responses. The Roman lines/strains of rats. Ann. N. Y. Acad. Sci., 1998, 851(1), 501-510.
[http://dx.doi.org/10.1111/j.1749-6632.1998.tb09029.x] [PMID: 9668644]
[115]
Fernández-Teruel, A.; Oliveras, I.; Cañete, T.; Rio-Álamos, C.; Tapias-Espinosa, C.; Sampedro-Viana, D.; Sánchez-González, A.; Sanna, F.; Torrubia, R.; González-Maeso, J.; Driscoll, P.; Morón, I.; Torres, C.; Aznar, S.; Tobeña, A.; Corda, M.G.; Giorgi, O. Neurobehavioral and neurodevelopmental profiles of a heuristic genetic model of differential schizophrenia- and addiction-relevant features: The RHA vs. RLA rats. Neurosci. Biobehav. Rev., 2021, 131, 597-617.
[http://dx.doi.org/10.1016/j.neubiorev.2021.09.042] [PMID: 34571119]
[116]
Steimer, T.; Driscoll, P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: Behavioural, neuroendocrine and developmental aspects. Stress, 2003, 6(2), 87-100.
[http://dx.doi.org/10.1080/1025389031000111320] [PMID: 12775328]
[117]
Steimer, T.; Driscoll, P. Inter-individual vs line/strain differences in psychogenetically selected Roman High-(RHA) and Low-(RLA) Avoidance rats: Neuroendocrine and behavioural aspects. Neurosci. Biobehav. Rev., 2005, 29(1), 99-112.
[http://dx.doi.org/10.1016/j.neubiorev.2004.07.002] [PMID: 15652258]
[118]
Sampedro-Viana, D.; Cañete, T.; Sanna, F.; Soley, B.; Giorgi, O.; Corda, M.G.; Torrecilla, P.; Oliveras, I.; Tapias-Espinosa, C.; Río-Álamos, C.; Sánchez-González, A.; Tobeña, A.; Fernández-Teruel, A. Decreased social interaction in the RHA rat model of schizophrenia-relevant features: Modulation by neonatal handling. Behav. Processes, 2021, 188, 104397.
[http://dx.doi.org/10.1016/j.beproc.2021.104397] [PMID: 33887361]
[119]
Oliveras, I.; Soria-Ruiz, O.J.; Sampedro-Viana, D.; Cañete, T.; Tobeña, A.; Fernández-Teruel, A. Social preference in Roman rats: Age and sex variations relevance for modeling negative schizophrenia-like features. Physiol. Behav., 2022, 247, 113722.
[http://dx.doi.org/10.1016/j.physbeh.2022.113722] [PMID: 35077728]
[120]
Driscoll, P.; Fümm, H.; Bättig, K. Maternal behavior in two rat lines selected for differences in the acquisition of two-way avoidance. Experientia, 1979, 35(6), 786-788.
[http://dx.doi.org/10.1007/BF01968248] [PMID: 467590]
[121]
Coppens, C.M.; de Boer, S.F.; Steimer, T.; Koolhaas, J.M. Correlated behavioral traits in rats of the Roman selection lines. Behav. Genet., 2013, 43(3), 220-226.
[http://dx.doi.org/10.1007/s10519-013-9588-8] [PMID: 23417785]
[122]
Oliveras, I.; Sánchez-González, A.; Sampedro-Viana, D.; Piludu, M.A.; Río-Alamos, C.; Giorgi, O.; Corda, M.G.; Aznar, S.; González-Maeso, J.; Gerbolés, C.; Blázquez, G.; Cañete, T.; Tobeña, A.; Fernández-Teruel, A. Differential effects of antipsychotic and propsychotic drugs on prepulse inhibition and locomotor activity in Roman high- (RHA) and low-avoidance (RLA) rats. Psychopharmacology (Berl.), 2017, 234(6), 957-975.
[http://dx.doi.org/10.1007/s00213-017-4534-8] [PMID: 28154892]
[123]
López-Aumatell, R.; Blázquez, G.; Gil, L.; Aguilar, R.; Cañete, T.; Giménez-Llort, L.; Tobeña, A.; Fernández-Teruel, A. The Roman High- and Low-Avoidance rat strains differ in fear-potentiated startle and classical aversive conditioning. Psicothema, 2009, 21(1), 27-32.
[PMID: 19178852]
[124]
Escorihuela, R.M.; Tobeña, A.; Fernández-Teruel, A. Environmental enrichment and postnatal handling prevent spatial learning deficits in aged hypoemotional (Roman high-avoidance) and hyperemotional (Roman low-avoidance) rats. Learn. Mem., 1995, 2(1), 40-48.
[http://dx.doi.org/10.1101/lm.2.1.40] [PMID: 10467565]
[125]
Nil, R.; Bättig, K. Spontaneous maze ambulation and Hebb-Williams learning in roman high-avoidance and roman low-avoidance rats. Behav. Neural Biol., 1981, 33(4), 465-475.
[http://dx.doi.org/10.1016/S0163-1047(81)91833-1] [PMID: 7332509]
[126]
Oliveras, I.; Sánchez-González, A.; Piludu, M.A.; Gerboles, C.; Río-Álamos, C.; Tobeña, A.; Fernández-Teruel, A. Divergent effects of isolation rearing on prepulse inhibition, activity, anxiety and hippocampal-dependent memory in Roman high- and low-avoidance rats: A putative model of schizophrenia-relevant features. Behav. Brain Res., 2016, 314, 6-15.
[http://dx.doi.org/10.1016/j.bbr.2016.07.047] [PMID: 27478139]
[127]
Willig, F.; M’Harzi, M.; Bardelay, C.; Viet, D.; Delacour, J. Roman strains as a psychogenetic model for the study of working memory: Behavioral and biochemical data. Pharmacol. Biochem. Behav., 1991, 40(1), 7-16.
[http://dx.doi.org/10.1016/0091-3057(91)90313-Q] [PMID: 1780348]
[128]
Zeier, H.; Baettig, K.; Driscoll, P. Acquisition of DRL-20 behavior in male and female, Roman high- and low-avoidance rats. Physiol. Behav., 1978, 20(6), 791-793.
[http://dx.doi.org/10.1016/0031-9384(78)90307-4] [PMID: 684114]
[129]
Coppens, C.M.; de Boer, S.F.; Steimer, T.; Koolhaas, J.M. Impulsivity and aggressive behavior in Roman high and low avoidance rats: Baseline differences and adolescent social stress induced changes. Physiol. Behav., 2012, 105(5), 1156-1160.
[http://dx.doi.org/10.1016/j.physbeh.2011.12.013] [PMID: 22212239]
[130]
Moreno, M.; Cardona, D.; Gómez, M.J.; Sánchez-Santed, F.; Tobeña, A.; Fernández-Teruel, A.; Campa, L.; Suñol, C.; Escarabajal, M.D.; Torres, C.; Flores, P. Impulsivity characterization in the Roman high- and low-avoidance rat strains: Behavioral and neurochemical differences. Neuropsychopharmacology, 2010, 35(5), 1198-1208.
[http://dx.doi.org/10.1038/npp.2009.224] [PMID: 20090672]
[131]
Esnal, A.; Sánchez-González, A.; Río-Álamos, C.; Oliveras, I.; Cañete, T.; Blázquez, G.; Tobeña, A.; Fernández-Teruel, A. Prepulse inhibition and latent inhibition deficits in Roman high-avoidance vs. Roman low-avoidance rats: Modeling schizophrenia-related features. Physiol. Behav., 2016, 163, 267-273.
[http://dx.doi.org/10.1016/j.physbeh.2016.05.020] [PMID: 27184235]
[132]
Fernández-Teruel, A.; Blázquez, G.; Pérez, M.; Aguilar, R.; Cañete, T.; Guitart, M.; Giménez-Llort, L.; Tobeña, A. Latent inhibition threshold in Roman high-avoidance rats: A psychogenetic model of abnormalities in attentional filter? Actas Esp. Psiquiatr., 2006, 34(4), 257-263.
[PMID: 16823687]
[133]
Oliveras, I.; Tapias-Espinosa, C.; Río-Álamos, C.; Sampedro-Viana, D.; Cañete, T.; Sánchez-González, A.; Tobeña, A.; Fernández-Teruel, A. Prepulse inhibition deficits in inbred and outbred rats and between-strain differences in startle habituation do not depend on startle reactivity levels. Behav. Processes, 2022, 197, 104618.
[http://dx.doi.org/10.1016/j.beproc.2022.104618] [PMID: 35259448]
[134]
Río-Álamos, C.; Piludu, M.A.; Gerbolés, C.; Barroso, D.; Oliveras, I.; Sánchez-González, A.; Cañete, T.; Tapias-Espinosa, C.; Sampedro-Viana, D.; Torrubia, R.; Tobeña, A.; Fernández-Teruel, A. Volumetric brain differences between the Roman rat strains: Neonatal handling effects, sensorimotor gating and working memory. Behav. Brain Res., 2019, 361, 74-85.
[http://dx.doi.org/10.1016/j.bbr.2018.12.033] [PMID: 30576720]
[135]
Tapias-Espinosa, C.; Cañete, T.; Sampedro-Viana, D.; Brudek, T.; Kaihøj, A.; Oliveras, I.; Tobeña, A.; Aznar, S.; Fernández-Teruel, A. Oxytocin attenuates schizophrenia-like reduced sensorimotor gating in outbred and inbred rats in line with strain differences in CD38 gene expression. Physiol. Behav., 2021, 240, 113547.
[http://dx.doi.org/10.1016/j.physbeh.2021.113547] [PMID: 34364851]
[136]
Elfving, B.; Müller, H.K.; Oliveras, I.; Østerbøg, T.B.; Rio-Alamos, C.; Sanchez-González, A.; Tobeña, A.; Fernández-Teruel, A.; Aznar, S. Differential expression of synaptic markers regulated during neurodevelopment in a rat model of schizophrenia-like behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2019, 95, 109669.
[http://dx.doi.org/10.1016/j.pnpbp.2019.109669] [PMID: 31228641]
[137]
Fomsgaard, L.; Moreno, J.L.; de la Fuente Revenga, M.; Brudek, T.; Adamsen, D.; Rio-Alamos, C.; Saunders, J.; Klein, A.B.; Oliveras, I.; Cañete, T.; Blazquez, G.; Tobeña, A.; Fernandez-Teruel, A.; Gonzalez-Maeso, J.; Aznar, S. Differences in 5-HT2A and mGlu2 receptor expression levels and repressive epigenetic modifications at the 5-HT2A promoter region in the roman low- (RLA-I) and high- (RHA-I) avoidance rat strains. Mol. Neurobiol., 2018, 55(3), 1998-2012.
[http://dx.doi.org/10.1007/s12035-017-0457-y] [PMID: 28265857]
[138]
Klein, A.B.; Ultved, L.; Adamsen, D.; Santini, M.A.; Tobeña, A.; Fernandez-Teruel, A.; Flores, P.; Moreno, M.; Cardona, D.; Knudsen, G.M.; Aznar, S.; Mikkelsen, J.D. 5-HT2A and mGlu2 receptor binding levels are related to differences in impulsive behavior in the roman low- (RLA) and high- (RHA) avoidance rat strains. Neuroscience, 2014, 263, 36-45.
[http://dx.doi.org/10.1016/j.neuroscience.2013.12.063] [PMID: 24412375]
[139]
Meyza, K.Z.; Boguszewski, P.M.; Nikolaev, E.; Zagrodzka, J. Diverse sensitivity of RHA/Verh and RLA/Verh rats to emotional and spatial aspects of a novel environment as a result of a distinct pattern of neuronal activation in the fear/anxiety circuit. Behav. Genet., 2009, 39(1), 48-61.
[http://dx.doi.org/10.1007/s10519-008-9234-z] [PMID: 18972198]
[140]
Río-Álamos, C.; Oliveras, I.; Piludu, M.A.; Gerbolés, C.; Cañete, T.; Blázquez, G.; Lope-Piedrafita, S.; Martínez-Membrives, E.; Torrubia, R.; Tobeña, A.; Fernández-Teruel, A. Neonatal handling enduringly decreases anxiety and stress responses and reduces hippocampus and amygdala volume in a genetic model of differential anxiety: Behavioral-volumetric associations in the Roman rat strains. Eur. Neuropsychopharmacol., 2017, 27(2), 146-158.
[http://dx.doi.org/10.1016/j.euroneuro.2016.12.003] [PMID: 28049558]
[141]
Sánchez-González, A.; Thougaard, E.; Tapias-Espinosa, C.; Cañete, T.; Sampedro-Viana, D.; Saunders, J.M.; Toneatti, R.; Tobeña, A.; Gónzalez-Maeso, J.; Aznar, S.; Fernández-Teruel, A. Increased thin-spine density in frontal cortex pyramidal neurons in a genetic rat model of schizophrenia-relevant features. Eur. Neuropsychopharmacol., 2021, 44, 79-91.
[http://dx.doi.org/10.1016/j.euroneuro.2021.01.006] [PMID: 33485732]
[142]
Aguilar, R.; Escorihuela, R.M.; Gil, L.; Tobeña, A.; Fernández-Teruel, A. Differences between two psychogenetically selected lines of rats in a swimming pool matching-to-place task: Long-term effects of infantile stimulation. Behav. Genet., 2002, 32(2), 127-134.
[http://dx.doi.org/10.1023/A:1015253807488] [PMID: 12036110]
[143]
Fone, K.C.F.; Porkess, M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents—Relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev., 2008, 32(6), 1087-1102.
[http://dx.doi.org/10.1016/j.neubiorev.2008.03.003] [PMID: 18423591]
[144]
Sánchez-González, A.; Oliveras, I.; Río-Álamos, C.; Piludu, M.A.; Gerbolés, C.; Tapias-Espinosa, C.; Tobeña, A.; Aznar, S.; Fernández-Teruel, A. Dissociation between schizophrenia-relevant behavioral profiles and volumetric brain measures after long-lasting social isolation in Roman rats. Neurosci. Res., 2020, 155, 43-55.
[http://dx.doi.org/10.1016/j.neures.2019.07.002] [PMID: 31306676]
[145]
Giménezllort, L.; Cañete, T.; Guitartmasip, M.; Fernándezteruel, A.; Tobeña, A. Two distinctive apomorphine-induced phenotypes in the Roman high- and low-avoidance rats. Physiol. Behav., 2005, 86(4), 458-466.
[http://dx.doi.org/10.1016/j.physbeh.2005.07.021] [PMID: 16154604]
[146]
Tapias-Espinosa, C.; Río-Álamos, C.; Sampedro-Viana, D.; Gerbolés, C.; Oliveras, I.; Sánchez-González, A.; Tobeña, A.; Fernández-Teruel, A. Increased exploratory activity in rats with deficient sensorimotor gating: A study of schizophrenia-relevant symptoms with genetically heterogeneous NIH-HS and Roman rat strains. Behav. Processes, 2018, 151, 96-103.
[http://dx.doi.org/10.1016/j.beproc.2018.03.019] [PMID: 29567400]
[147]
Schwabe, K.; Polikashvili, N.; Krauss, J.K. Deficient sensorimotor gating induced by selective breeding in rats is improved by entopeduncular nucleus lesions. Neurobiol. Dis., 2009, 34(2), 351-356.
[http://dx.doi.org/10.1016/j.nbd.2009.02.004] [PMID: 19233272]
[148]
Horvath, G.; Kekesi, G.; Petrovszki, Z.; Benedek, G. Abnormal motor activity and thermoregulation in a schizophrenia rat model for translational science. PLoS One, 2015, 10(12), e0143751.
[http://dx.doi.org/10.1371/journal.pone.0143751] [PMID: 26629908]
[149]
Corda, M.G.; Piras, G.; Lecca, D.; Fernández-Teruel, A.; Driscoll, P.; Giorgi, O. The psychogenetically selected Roman rat lines differ in the susceptibility to develop amphetamine sensitization. Behav. Brain Res., 2005, 157(1), 147-156.
[http://dx.doi.org/10.1016/j.bbr.2004.06.016] [PMID: 15617781]
[150]
Giorgi, O.; Piras, G.; Lecca, D.; Corda, M.G. Behavioural effects of acute and repeated cocaine treatments: A comparative study in sensitisation-prone RHA rats and their sensitisation-resistant RLA counterparts. Psychopharmacology (Berl.), 2005, 180(3), 530-538.
[http://dx.doi.org/10.1007/s00213-005-2177-7] [PMID: 15772864]
[151]
Amini, B.; Yang, P.B.; Swann, A.C.; Dafny, N. Differential locomotor responses in male rats from three strains to acute methylphenidate. Int. J. Neurosci., 2004, 114(9), 1063-1084.
[http://dx.doi.org/10.1080/00207450490475526] [PMID: 15370174]
[152]
Fodor, A.; Klausz, B.; Toth, B.; Zelena, D. The prepulse inhibition deficit appearance is largely independent on the circadian cycle, body weight, and the gender of vasopressin deficient Brattleboro rat. Endocr. Regul., 2016, 50(1), 16-23.
[http://dx.doi.org/10.1515/enr-2016-0004] [PMID: 27560632]
[153]
Feifel, D.; Shilling, P.D.; Fazlinejad, A.A.; Melendez, G. Antipsychotic drug-like facilitation of latent inhibition by a brain-penetrating neurotensin-1 receptor agonist. J. Psychopharmacol., 2016, 30(3), 312-317.
[http://dx.doi.org/10.1177/0269881115625360] [PMID: 26783230]
[154]
Fernández-Teruel, A.; Escorihuela, R.M.; Castellano, B.; González, B.; Tobeña, A. Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: Focus on the Roman rat lines. Behav. Genet., 1997, 27(6), 513-526.
[http://dx.doi.org/10.1023/A:1021400830503] [PMID: 9476360]
[155]
Coppens, C.M.; de Boer, S.F.; Koolhaas, J.M. Coping styles and behavioural flexibility: Towards underlying mechanisms. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2010, 365(1560), 4021-4028.
[http://dx.doi.org/10.1098/rstb.2010.0217] [PMID: 21078654]
[156]
López-Aumatell, R.; Vicens-Costa, E.; Guitart-Masip, M.; Martínez-Membrives, E.; Valdar, W.; Johannesson, M.; Cañete, T.; Blázquez, G.; Driscoll, P.; Flint, J.; Tobeña, A.; Fernández-Teruel, A. Unlearned anxiety predicts learned fear: A comparison among heterogeneous rats and the Roman rat strains. Behav. Brain Res., 2009, 202(1), 92-101.
[http://dx.doi.org/10.1016/j.bbr.2009.03.024] [PMID: 19447285]
[157]
Schatz, K.C.; Kyne, R.F.; Parmeter, S.L.; Paul, M.J. Investigation of social, affective, and locomotor behavior of adolescent Brattleboro rats reveals a link between vasopressin’s actions on arousal and social behavior. Horm. Behav., 2018, 106, 1-9.
[http://dx.doi.org/10.1016/j.yhbeh.2018.08.015] [PMID: 30184461]
[158]
Engelmann, M.; Landgraf, R. Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats. Physiol. Behav., 1994, 55(1), 145-149.
[http://dx.doi.org/10.1016/0031-9384(94)90022-1] [PMID: 8140159]
[159]
Schank, J. Early locomotor and social effects in vasopressin deficient neonatal rats. Behav. Brain Res., 2009, 197(1), 166-177.
[http://dx.doi.org/10.1016/j.bbr.2008.08.019] [PMID: 18786571]
[160]
Paul, M.J.; Peters, N.V.; Holder, M.K.; Kim, A.M.; Whylings, J.; Terranova, J.I.; de Vries, G.J. Atypical social development in vasopressin- deficient brattleboro rats. eNeuro, 2016, 3(2), ENEURO.0150-15.2016.
[http://dx.doi.org/10.1523/ENEURO.0150-15.2016]
[161]
Aliczki, M.; Fodor, A.; Balogh, Z.; Haller, J.; Zelena, D. The effects of lactation on impulsive behavior in vasopressin-deficient Brattleboro rats. Horm. Behav., 2014, 66(3), 545-551.
[http://dx.doi.org/10.1016/j.yhbeh.2014.08.002] [PMID: 25117459]
[162]
Sanabria, F.; Killeen, P.R. Evidence for impulsivity in the spontaneously hypertensive rat drawn from complementary response-withholding tasks. Behav. Brain Funct., 2008, 4(1), 7.
[http://dx.doi.org/10.1186/1744-9081-4-7] [PMID: 18261220]
[163]
Orduña, V.; Mercado, E., III Impulsivity in spontaneously hypertensive rats: Within-subjects comparison of sensitivity to delay and to amount of reinforcement. Behav. Brain Res., 2017, 328, 178-185.
[http://dx.doi.org/10.1016/j.bbr.2017.04.033] [PMID: 28435126]
[164]
Tournier, B.B.; Steimer, T.; Millet, P.; Moulin-Sallanon, M.; Vallet, P.; Ibañez, V.; Ginovart, N. Innately low D2 receptor availability is associated with high novelty-seeking and enhanced behavioural sensitization to amphetamine. Int. J. Neuropsychopharmacol., 2013, 16(8), 1819-1834.
[http://dx.doi.org/10.1017/S1461145713000205] [PMID: 23574629]
[165]
Fattore, L.; Piras, G.; Corda, M.G.; Giorgi, O. The Roman high- and low-avoidance rat lines differ in the acquisition, maintenance, extinction, and reinstatement of intravenous cocaine self-administration. Neuropsychopharmacology, 2009, 34(5), 1091-1101.
[http://dx.doi.org/10.1038/npp.2008.43] [PMID: 18418365]
[166]
Corda, M.G.; Piras, G.; Piludu, M.A.; Giorgi, O. Differential effects of voluntary ethanol consumption on dopamine output in the nucleus accumbens shell of roman high- and low-avoidance rats: A behavioral and brain microdialysis study. World J. Neurosci., 2014, 4(3), 279-292.
[http://dx.doi.org/10.4236/wjns.2014.43031]
[167]
Ellenbroek, B.A.; van der Kam, E.L.; van der Elst, M.C.J.; Cools, A.R. Individual differences in drug dependence in rats: The role of genetic factors and life events. Eur. J. Pharmacol., 2005, 526(1-3), 251-258.
[http://dx.doi.org/10.1016/j.ejphar.2005.09.032] [PMID: 16253227]
[168]
Giorgi, O.; Orlandi, M.; Escorihuela, R.M.; Driscoll, P.; Lecca, D.; Corda, M.G. GABAergic and dopaminergic transmission in the brain of Roman high-avoidance and Roman low-avoidance rats. Brain Res., 1994, 638(1-2), 133-138.
[http://dx.doi.org/10.1016/0006-8993(94)90642-4] [PMID: 8199854]
[169]
Guitart-Masip, M.; Johansson, B.; Fernández-Teruel, A.; Cañete, T.; Tobeña, A.; Terenius, L.; Giménez-Llort, L. Divergent anatomical pattern of D1 and D3 binding and dopamine- and cyclic AMP-regulated phosphoprotein of 32 kDa mRNA expression in the Roman rat strains: Implications for drug addiction. Neuroscience, 2006, 142(4), 1231-1243.
[http://dx.doi.org/10.1016/j.neuroscience.2006.07.041] [PMID: 17008016]
[170]
Sanna, F.; Bratzu, J.; Piludu, M.A.; Corda, M.G.; Melis, M.R.; Giorgi, O.; Argiolas, A. Dopamine, noradrenaline and differences in sexual behavior between Roman high and low avoidance male rats: A microdialysis study in the medial prefrontal cortex. Front. Behav. Neurosci., 2017, 11, 108.
[http://dx.doi.org/10.3389/fnbeh.2017.00108] [PMID: 28638325]
[171]
Driscoll, P.; Dedek, J.; Martin, J.R.; Baettig, K. Regional 5-HT analysis in roman high- and low-avoidance rats following MAO inhibition. Eur. J. Pharmacol., 1980, 68(3), 373-376.
[http://dx.doi.org/10.1016/0014-2999(80)90536-1] [PMID: 6162652]
[172]
Giorgi, O.; Piras, G.; Lecca, D.; Hansson, S.; Driscoll, P.; Corda, M.G. Differential neurochemical properties of central serotonergic transmission in Roman high- and low-avoidance rats. J. Neurochem., 2003, 86(2), 422-431.
[http://dx.doi.org/10.1046/j.1471-4159.2003.01845.x] [PMID: 12871583]
[173]
Charnay, Y.; Steimer, T.; Huguenin, C.; Driscoll, P. [3H] Paroxetine binding sites: Brain regional differences between two psychogenetically selected lines of rats. Neurosci. Res. Commun., 1995, 16(1), 29-35.
[174]
Valdez, S.; Li, J-Y.; Mazor, R.; Kuo, T.; Schmid-Schönbein, G. Sleep pattern and serotonin 5HT-1A receptor cleavage in the brain of the spontaneously hypertensive rat. FASEB J., 2011, 25(S1), 640.38.
[175]
Garcia-Falgueras, A.; Castillo-Ruiz, M.M.; Put, T.; Tobeña, A.; Fernández-Teruel, A. Differential hippocampal neuron density between inbred Roman high- (low anxious) and low-avoidance (high anxious) rats. Neurosci. Lett., 2012, 522(1), 41-46.
[http://dx.doi.org/10.1016/j.neulet.2012.06.011] [PMID: 22698586]
[176]
Gómez, M.J.; Morón, I.; Torres, C.; Esteban, F.J.; de la Torre, L.; Cándido, A.; Maldonado, A.; Fernández-Teruel, A.; Tobeña, A.; Escarabajal, M.D. One-way avoidance acquisition and cellular density in the basolateral amygdala: Strain differences in Roman high- and low-avoidance rats. Neurosci. Lett., 2009, 450(3), 317-320.
[http://dx.doi.org/10.1016/j.neulet.2008.10.112] [PMID: 19056466]
[177]
Piras, G.; Lecca, D.; Corda, M.G.; Giorgi, O. Repeated morphine injections induce behavioural sensitization in Roman high- but not in Roman low-avoidance rats. Neuroreport, 2003, 14(18), 2433-2438.
[http://dx.doi.org/10.1097/00001756-200312190-00029] [PMID: 14663206]
[178]
Buckley, P.F.; Miller, B.J.; Lehrer, D.S.; Castle, D.J. Psychiatric comorbidities and schizophrenia. Schizophr. Bull., 2009, 35(2), 383-402.
[http://dx.doi.org/10.1093/schbul/sbn135] [PMID: 19011234]
[179]
Gøtzsche, P.C. Deadly medicines and organised crime: How big pharma has corrupted healthcare; Radcliffe Publishing: England, UK, 2014.
[180]
Gøtzsche, P.C. Deadly psychiatry and organised denial: Art People: Copenhague; , 2015.
[181]
Anderzhanova, E.; Kirmeier, T.; Wotjak, C.T. Animal models in psychiatric research: The RDoC system as a new framework for endophenotype-oriented translational neuroscience. Neurobiol. Stress, 2017, 7, 47-56.
[http://dx.doi.org/10.1016/j.ynstr.2017.03.003] [PMID: 28377991]
[182]
Insel, T.; Cuthbert, B.; Garvey, M.; Heinssen, R.; Pine, D.S.; Quinn, K.; Sanislow, C.; Wang, P. Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. Am. J. Psychiatry, 2010, 167(7), 748-751.
[http://dx.doi.org/10.1176/appi.ajp.2010.09091379] [PMID: 20595427]
[183]
Yolland, C.O.B.; Phillipou, A.; Castle, D.J.; Neill, E.; Hughes, M.E.; Galletly, C.; Smith, Z.M.; Francis, P.S.; Dean, O.M.; Sarris, J.; Siskind, D.; Harris, A.W.F.; Rossell, S.L. Improvement of cognitive function in schizophrenia with N -acetylcysteine: A theoretical review. Nutr. Neurosci., 2020, 23(2), 139-148.
[http://dx.doi.org/10.1080/1028415X.2018.1478766] [PMID: 29847303]
[184]
Singh, T.; Poterba, T.; Curtis, D.; Akil, H.; Al Eissa, M.; Barchas, J.D.; Bass, N.; Bigdeli, T.B.; Breen, G.; Bromet, E.J.; Buckley, P.F.; Bunney, W.E.; Bybjerg-Grauholm, J.; Byerley, W.F.; Chapman, S.B.; Chen, W.J.; Churchhouse, C.; Craddock, N.; Cusick, C.M.; DeLisi, L.; Dodge, S.; Escamilla, M.A.; Eskelinen, S.; Fanous, A.H.; Faraone, S.V.; Fiorentino, A.; Francioli, L.; Gabriel, S.B.; Gage, D.; Gagliano Taliun, S.A.; Ganna, A.; Genovese, G.; Glahn, D.C.; Grove, J.; Hall, M.H.; Hämäläinen, E.; Heyne, H.O.; Holi, M.; Hougaard, D.M.; Howrigan, D.P.; Huang, H.; Hwu, H.G.; Kahn, R.S.; Kang, H.M.; Karczewski, K.J.; Kirov, G.; Knowles, J.A.; Lee, F.S.; Lehrer, D.S.; Lescai, F.; Malaspina, D.; Marder, S.R.; McCarroll, S.A.; McIntosh, A.M.; Medeiros, H.; Milani, L.; Morley, C.P.; Morris, D.W.; Mortensen, P.B.; Myers, R.M.; Nordentoft, M.; O’Brien, N.L.; Olivares, A.M.; Ongur, D.; Ouwehand, W.H.; Palmer, D.S.; Paunio, T.; Quested, D.; Rapaport, M.H.; Rees, E.; Rollins, B.; Satterstrom, F.K.; Schatzberg, A.; Scolnick, E.; Scott, L.J.; Sharp, S.I.; Sklar, P.; Smoller, J.W.; Sobell, J.L.; Solomonson, M.; Stahl, E.A.; Stevens, C.R.; Suvisaari, J.; Tiao, G.; Watson, S.J.; Watts, N.A.; Blackwood, D.H.; Børglum, A.D.; Cohen, B.M.; Corvin, A.P.; Esko, T.; Freimer, N.B.; Glatt, S.J.; Hultman, C.M.; McQuillin, A.; Palotie, A.; Pato, C.N.; Pato, M.T.; Pulver, A.E.; St Clair, D.; Tsuang, M.T.; Vawter, M.P.; Walters, J.T.; Werge, T.M.; Ophoff, R.A.; Sullivan, P.F.; Owen, M.J.; Boehnke, M.; O’Donovan, M.C.; Neale, B.M.; Daly, M.J. Rare coding variants in ten genes confer substantial risk for schizophrenia. Nature, 2022, 604(7906), 509-516.
[http://dx.doi.org/10.1038/s41586-022-04556-w] [PMID: 35396579]
[185]
Trubetskoy, V.; Pardiñas, A.F.; Qi, T.; Panagiotaropoulou, G.; Awasthi, S.; Bigdeli, T.B.; Bryois, J.; Chen, C.Y.; Dennison, C.A.; Hall, L.S.; Lam, M.; Watanabe, K.; Frei, O.; Ge, T.; Harwood, J.C.; Koopmans, F.; Magnusson, S.; Richards, A.L.; Sidorenko, J.; Wu, Y.; Zeng, J.; Grove, J.; Kim, M.; Li, Z.; Voloudakis, G.; Zhang, W.; Adams, M.; Agartz, I.; Atkinson, E.G.; Agerbo, E.; Al Eissa, M.; Albus, M.; Alexander, M.; Alizadeh, B.Z.; Alptekin, K.; Als, T.D.; Amin, F.; Arolt, V.; Arrojo, M.; Athanasiu, L.; Azevedo, M.H.; Bacanu, S.A.; Bass, N.J.; Begemann, M.; Belliveau, R.A.; Bene, J.; Benyamin, B.; Bergen, S.E.; Blasi, G.; Bobes, J.; Bonassi, S.; Braun, A.; Bressan, R.A.; Bromet, E.J.; Bruggeman, R.; Buckley, P.F.; Buckner, R.L.; Bybjerg-Grauholm, J.; Cahn, W.; Cairns, M.J.; Calkins, M.E.; Carr, V.J.; Castle, D.; Catts, S.V.; Chambert, K.D.; Chan, R.C.K.; Chaumette, B.; Cheng, W.; Cheung, E.F.C.; Chong, S.A.; Cohen, D.; Consoli, A.; Cordeiro, Q.; Costas, J.; Curtis, C.; Davidson, M.; Davis, K.L.; de Haan, L.; Degenhardt, F.; DeLisi, L.E.; Demontis, D.; Dickerson, F.; Dikeos, D.; Dinan, T.; Djurovic, S.; Duan, J.; Ducci, G.; Dudbridge, F.; Eriksson, J.G.; Fañanás, L.; Faraone, S.V.; Fiorentino, A.; Forstner, A.; Frank, J.; Freimer, N.B.; Fromer, M.; Frustaci, A.; Gadelha, A.; Genovese, G.; Gershon, E.S.; Giannitelli, M.; Giegling, I.; Giusti-Rodríguez, P.; Godard, S.; Goldstein, J.I.; González Peñas, J.; González-Pinto, A.; Gopal, S.; Gratten, J.; Green, M.F.; Greenwood, T.A.; Guillin, O.; Gülöksüz, S.; Gur, R.E.; Gur, R.C.; Gutiérrez, B.; Hahn, E.; Hakonarson, H.; Haroutunian, V.; Hartmann, A.M.; Harvey, C.; Hayward, C.; Henskens, F.A.; Herms, S.; Hoffmann, P.; Howrigan, D.P.; Ikeda, M.; Iyegbe, C.; Joa, I.; Julià, A.; Kähler, A.K.; Kam-Thong, T.; Kamatani, Y.; Karachanak-Yankova, S.; Kebir, O.; Keller, M.C.; Kelly, B.J.; Khrunin, A.; Kim, S.W.; Klovins, J.; Kondratiev, N.; Konte, B.; Kraft, J.; Kubo, M.; Kučinskas, V.; Kučinskiene, Z.A.; Kusumawardhani, A.; Kuzelova-Ptackova, H.; Landi, S.; Lazzeroni, L.C.; Lee, P.H.; Legge, S.E.; Lehrer, D.S.; Lencer, R.; Lerer, B.; Li, M.; Lieberman, J.; Light, G.A.; Limborska, S.; Liu, C.M.; Lönnqvist, J.; Loughland, C.M.; Lubinski, J.; Luykx, J.J.; Lynham, A.; Macek, M., Jr; Mackinnon, A.; Magnusson, P.K.E.; Maher, B.S.; Maier, W.; Malaspina, D.; Mallet, J.; Marder, S.R.; Marsal, S.; Martin, A.R.; Martorell, L.; Mattheisen, M.; McCarley, R.W.; McDonald, C.; McGrath, J.J.; Medeiros, H.; Meier, S.; Melegh, B.; Melle, I.; Mesholam-Gately, R.I.; Metspalu, A.; Michie, P.T.; Milani, L.; Milanova, V.; Mitjans, M.; Molden, E.; Molina, E.; Molto, M.D.; Mondelli, V.; Moreno, C.; Morley, C.P.; Muntané, G.; Murphy, K.C.; Myin-Germeys, I.; Nenadić, I.; Nestadt, G.; Nikitina-Zake, L.; Noto, C.; Nuechterlein, K.H.; O’Brien, N.L.; O’Neill, F.A.; Oh, S.Y.; Olincy, A.; Ota, V.K.; Pantelis, C.; Papadimitriou, G.N.; Parellada, M.; Paunio, T.; Pellegrino, R.; Periyasamy, S.; Perkins, D.O.; Pfuhlmann, B.; Pietiläinen, O.; Pimm, J.; Porteous, D.; Powell, J.; Quattrone, D.; Quested, D.; Radant, A.D.; Rampino, A.; Rapaport, M.H.; Rautanen, A.; Reichenberg, A.; Roe, C.; Roffman, J.L.; Roth, J.; Rothermundt, M.; Rutten, B.P.F.; Saker-Delye, S.; Salomaa, V.; Sanjuan, J.; Santoro, M.L.; Savitz, A.; Schall, U.; Scott, R.J.; Seidman, L.J.; Sharp, S.I.; Shi, J.; Siever, L.J.; Sigurdsson, E.; Sim, K.; Skarabis, N.; Slominsky, P.; So, H.C.; Sobell, J.L.; Söderman, E.; Stain, H.J.; Steen, N.E.; Steixner-Kumar, A.A.; Stögmann, E.; Stone, W.S.; Straub, R.E.; Streit, F.; Strengman, E.; Stroup, T.S.; Subramaniam, M.; Sugar, C.A.; Suvisaari, J.; Svrakic, D.M.; Swerdlow, N.R.; Szatkiewicz, J.P.; Ta, T.M.T.; Takahashi, A.; Terao, C.; Thibaut, F.; Toncheva, D.; Tooney, P.A.; Torretta, S.; Tosato, S.; Tura, G.B.; Turetsky, B.I.; Üçok, A.; Vaaler, A.; van Amelsvoort, T.; van Winkel, R.; Veijola, J.; Waddington, J.; Walter, H.; Waterreus, A.; Webb, B.T.; Weiser, M.; Williams, N.M.; Witt, S.H.; Wormley, B.K.; Wu, J.Q.; Xu, Z.; Yolken, R.; Zai, C.C.; Zhou, W.; Zhu, F.; Zimprich, F.; Atbaşoğlu, E.C.; Ayub, M.; Benner, C.; Bertolino, A.; Black, D.W.; Bray, N.J.; Breen, G.; Buccola, N.G.; Byerley, W.F.; Chen, W.J.; Cloninger, C.R.; Crespo-Facorro, B.; Donohoe, G.; Freedman, R.; Galletly, C.; Gandal, M.J.; Gennarelli, M.; Hougaard, D.M.; Hwu, H.G.; Jablensky, A.V.; McCarroll, S.A.; Moran, J.L.; Mors, O.; Mortensen, P.B.; Müller-Myhsok, B.; Neil, A.L.; Nordentoft, M.; Pato, M.T.; Petryshen, T.L.; Pirinen, M.; Pulver, A.E.; Schulze, T.G.; Silverman, J.M.; Smoller, J.W.; Stahl, E.A.; Tsuang, D.W.; Vilella, E.; Wang, S.H.; Xu, S.; Dai, N.; Wenwen, Q.; Wildenauer, D.B.; Agiananda, F.; Amir, N.; Antoni, R.; Arsianti, T.; Asmarahadi, A.; Diatri, H.; Djatmiko, P.; Irmansyah, I.; Khalimah, S.; Kusumadewi, I.; Kusumaningrum, P.; Lukman, P.R.; Nasrun, M.W.; Safyuni, N.S.; Prasetyawan, P.; Semen, G.; Siste, K.; Tobing, H.; Widiasih, N.; Wiguna, T.; Wulandari, D.; Evalina, N.; Hananto, A.J.; Ismoyo, J.H.; Marini, T.M.; Henuhili, S.; Reza, M.; Yusnadewi, S.; Abyzov, A.; Akbarian, S.; Ashley-Koch, A.; van Bakel, H.; Breen, M.; Brown, M.; Bryois, J.; Carlyle, B.; Charney, A.; Coetzee, G.; Crawford, G.; Dracheva, S.; Emani, P.; Farnham, P.; Fromer, M.; Galeev, T.; Gandal, M.; Gerstein, M.; Giase, G.; Girdhar, K.; Goes, F.; Grennan, K.; Gu, M.; Guerra, B.; Gursoy, G.; Hoffman, G.; Hyde, T.; Jaffe, A.; Jiang, S.; Jiang, Y.; Kefi, A.; Kim, Y.; Kitchen, R.; Knowles, J.A.; Lay, F.; Lee, D.; Li, M.; Liu, C.; Liu, S.; Mattei, E.; Navarro, F.; Pan, X.; Peters, M.A.; Pinto, D.; Pochareddy, S.; Polioudakis, D.; Purcaro, M.; Purcell, S.; Pratt, H.; Reddy, T.; Rhie, S.; Roussos, P.; Rozowsky, J.; Sanders, S.; Sestan, N.; Sethi, A.; Shi, X.; Shieh, A.; Swarup, V.; Szekely, A.; Wang, D.; Warrell, J.; Weissman, S.; Weng, Z.; White, K.; Wiseman, J.; Witt, H.; Won, H.; Wood, S.; Wu, F.; Xu, X.; Yao, L.; Zandi, P.; Arranz, M.J.; Bakker, S.; Bender, S.; Bramon, E.; Collier, D.A.; Crepo-Facorro, B.; Hall, J.; Iyegbe, C.; Kahn, R.; Lawrie, S.; Lewis, C.; Lin, K.; Linszen, D.H.; Mata, I.; McIntosh, A.; Murray, R.M.; Ophoff, R.A.; van Os, J.; Powell, J.; Rujescu, D.; Walshe, M.; Weisbrod, M.; Achsel, T.; Andres-Alonso, M.; Bagni, C.; Bayés, À.; Biederer, T.; Brose, N.; Brown, T.C.; Chua, J.J.E.; Coba, M.P.; Cornelisse, L.N.; de Jong, A.P.H.; de Juan-Sanz, J.; Dieterich, D.C.; Feng, G.; Goldschmidt, H.L.; Gundelfinger, E.D.; Hoogenraad, C.; Huganir, R.L.; Hyman, S.E.; Imig, C.; Jahn, R.; Jung, H.; Kaeser, P.S.; Kim, E.; Koopmans, F.; Kreutz, M.R.; Lipstein, N.; MacGillavry, H.D.; Malenka, R.; McPherson, P.S.; O’Connor, V.; Pielot, R.; Ryan, T.A.; Sahasrabudhe, D.; Sala, C.; Sheng, M.; Smalla, K-H.; Smit, A.B.; Südhof, T.C.; Thomas, P.D.; Toonen, R.F.; van Weering, J.R.T.; Verhage, M.; Verpelli, C.; Adolfsson, R.; Arango, C.; Baune, B.T.; Belangero, S.I.; Børglum, A.D.; Braff, D.; Bramon, E.; Buxbaum, J.D.; Campion, D.; Cervilla, J.A.; Cichon, S.; Collier, D.A.; Corvin, A.; Curtis, D.; Forti, M.D.; Domenici, E.; Ehrenreich, H.; Escott-Price, V.; Esko, T.; Fanous, A.H.; Gareeva, A.; Gawlik, M.; Gejman, P.V.; Gill, M.; Glatt, S.J.; Golimbet, V.; Hong, K.S.; Hultman, C.M.; Hyman, S.E.; Iwata, N.; Jönsson, E.G.; Kahn, R.S.; Kennedy, J.L.; Khusnutdinova, E.; Kirov, G.; Knowles, J.A.; Krebs, M-O.; Laurent-Levinson, C.; Lee, J.; Lencz, T.; Levinson, D.F.; Li, Q.S.; Liu, J.; Malhotra, A.K.; Malhotra, D.; McIntosh, A.; McQuillin, A.; Menezes, P.R.; Morgan, V.A.; Morris, D.W.; Mowry, B.J.; Murray, R.M.; Nimgaonkar, V.; Nöthen, M.M.; Ophoff, R.A.; Paciga, S.A.; Palotie, A.; Pato, C.N.; Qin, S.; Rietschel, M.; Riley, B.P.; Rivera, M.; Rujescu, D.; Saka, M.C.; Sanders, A.R.; Schwab, S.G.; Serretti, A.; Sham, P.C.; Shi, Y.; St Clair, D.; Stefánsson, H.; Stefansson, K.; Tsuang, M.T.; van Os, J.; Vawter, M.P.; Weinberger, D.R.; Werge, T.; Wildenauer, D.B.; Yu, X.; Yue, W.; Holmans, P.A.; Pocklington, A.J.; Roussos, P.; Vassos, E.; Verhage, M.; Visscher, P.M.; Yang, J.; Posthuma, D.; Andreassen, O.A.; Kendler, K.S.; Owen, M.J.; Wray, N.R.; Daly, M.J.; Huang, H.; Neale, B.M.; Sullivan, P.F.; Ripke, S.; Walters, J.T.R.; O’Donovan, M.C.; de Haan, L.; van Amelsvoort, T.; van Winkel, R.; Gareeva, A.; Sham, P.C.; Shi, Y.; St Clair, D.; van Os, J. Mapping genomic loci implicates genes and synaptic biology in schizophrenia. Nature, 2022, 604(7906), 502-508. [http://dx.doi.org/10.1038/s41586-022-04434-5]. [PMID: 35396580].
[186]
Hengartner, M.P.; Moncrieff, J. Inconclusive evidence in support of the dopamine hypothesis of psychosis: Why neurobiological research must consider medication use, adjust for important confounders, choose stringent comparators, and use larger samples. Front. Psychiatry, 2018, 9, 174.
[http://dx.doi.org/10.3389/fpsyt.2018.00174] [PMID: 29765340]
[187]
Moncrieff, J. A critique of the dopamine hypothesis of schizophrenia and psychosis. Harv. Rev. Psychiatry, 2009, 17(3), 214-225.
[http://dx.doi.org/10.1080/10673220902979896] [PMID: 19499420]
[188]
Howes, O.D.; Kapur, S. The dopamine hypothesis of schizophrenia: Version III--the final common pathway. Schizophr. Bull., 2009, 35(3), 549-562.
[http://dx.doi.org/10.1093/schbul/sbp006] [PMID: 19325164]
[189]
Howes, O.D.; Shatalina, E. Integrating the neurodevelopmental and dopamine hypotheses of schizophrenia and the role of cortical excitation-inhibition balance. Biol. Psychiatry, 2022, 92(6), 501-513.
[http://dx.doi.org/10.1016/j.biopsych.2022.06.017] [PMID: 36008036]
[190]
Millard, S.J.; Bearden, C.E.; Karlsgodt, K.H.; Sharpe, M.J. The prediction-error hypothesis of schizophrenia: New data point to circuit-specific changes in dopamine activity. Neuropsychopharmacology, 2022, 47(3), 628-640.
[http://dx.doi.org/10.1038/s41386-021-01188-y] [PMID: 34588607]
[191]
Tricklebank, M.D.; Tamminga, C.; Grottick, A.; Llorca, P.M.; Gatti McArthur, S.; Martel, J.C. Editorial: Dopaminergic alterations in schizophrenia. Front. Neurosci., 2021, 15, 663245.
[http://dx.doi.org/10.3389/fnins.2021.663245] [PMID: 33776646]
[192]
Seeman, M.V. History of the dopamine hypothesis of antipsychotic action. World J. Psychiatry, 2021, 11(7), 355-364.
[http://dx.doi.org/10.5498/wjp.v11.i7.355] [PMID: 34327128]

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