Forebrain gene expression predicts deficits in sensorimotor gating after isolation rearing in male rats

Behavioural Brain Research

Volumn 257, Issue , 2013, Pages 118-128

  Swerdlow, Neal R ^a   Light, Gregory A ^a,b   Trim, Ryan S ^a,b   Breier, Michelle R ^a   Hines, Samantha R ^a   Powell, Susan B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Catechol O methyltransferase; Isolation rearing; Medial prefrontal cortex; Nucleus accumbens; Prepulse inhibition; Schizophrenia

Indexed keywords

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; COMT GENE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ERBB4 GENE; EVOKED AUDITORY RESPONSE; FEMALE; FOREBRAIN; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GRID2 GENE; LIFE EVENT; LOCAL FIELD POTENTIAL; MALE; MOTOR DYSFUNCTION; MPFC GENE; NCAM1 GENE; NEUROPHYSIOLOGY; NEUROPSYCHOLOGY; NONHUMAN; NRG1 GENE; NUCLEUS ACCUMBENS; PREDICTION; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; REARING; REFLEX DISORDER; RELN GENE; REVIEW; SCHIZOPHRENIA; SENSORIMOTOR FUNCTION; SENSORY DYSFUNCTION; SENSORY GATING; SLC1A2 GENE; STARTLE REFLEX;

CATECHOL-O-METHYLTRANSFERASE; ISOLATION REARING; MEDIAL PREFRONTAL CORTEX; NUCLEUS ACCUMBENS; PREPULSE INHIBITION; SCHIZOPHRENIA;

ACOUSTIC STIMULATION; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; LAMENESS, ANIMAL; MALE; PROSENCEPHALON; RATS; SOCIAL ISOLATION; STARTLE REACTION;

EID: 84886304006     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.09.005     Document Type: Review

References (41)

1. Fone K.C., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 2008, 3:1087-1102.
2. Powell S.B. Models of neurodevelopmental abnormalities in schizophrenia. Curr Top Behav Neurosci 2010, 4:435-481.
3. Cilia J., Reavill C., Hagan J.J., Jones D.N. Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats. Psychopharmacology (Berl) 2001, 156:327-337.
4. Geyer M.A., Wilkinson L.S., Humby T., Robbins T.W. Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol Psychiatry 1993, 34:361-372.
5. Stevens K.E., Johnson R.G., Rose G.M. Rats reared in social isolation show schizophrenia-like changes in auditory gating. Pharmacol Biochem Behav 1997, 58:1031-1036.
6. 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.
7. Powell S.B., Geyer M.A., Preece M.A., Pitcher L.K., Reynolds G.P., Swerdlow N.R. Dopamine depletion of the nucleus accumbens reverses isolation-induced deficits in prepulse inhibition in rats. Neuroscience 2003, 119:233-240.
8. Day-Wilson K.M., Jones D.N., Southam E., Cilia J., Totterdell S. Medial prefrontal cortex volume loss in rats with isolation rearing-induced deficits in prepulse inhibition of acoustic startle. Neuroscience 2006, 141:1113-1121.
9. Krolow R., Noschang C., Weis S.N., Pettenuzzo L.F., Huffell A.P., Arcego D.M., Marcolin M., Mota C.S., Kolling J., Scherer E.B., Wyse A.T., Dalmaz C. Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex. Neurochem Res 2012, 37:1063-1073.
10. Hermes G., Li N., Duman C., Duman R. Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol Behav 2011, 104:354-359.
11. Turnock-Jones J.J., Jennings C.A., Robbins M.J., Cluderay J.E., Cilia J., Reid J.L., Taylor A., Jones D.N., Emson P.C., Southam E. Increased expression of the NR2A NMDA receptor subunit in the prefrontal cortex of rats reared in isolation. Synapse 2009, 63:836-846. 10.1002/syn.20665.
12. Murphy K.J., Ter Horst J.P., Cassidy A.W., DeSouza I.E., Morgunova M., Li C., Connole L.M., O'Sullivan N.C., Loscher J.S., Brady A.T., Rombach N., Connellan J., McGettigan P.A., Scully D., Fedriani R., Lukasz B., Moran M.P., McCabe O.M., Wantuch C.M., Hughes Z.A., Mulvany S.K., Higgins D.G., Pangalos M.N., Marquis K.L., O'Connor W.T., Ring R.H., von Schack D., Regan C.M. Temporal dysregulation of cortical gene expression in the isolation reared Wistar rat. J Neurochem 2010, 113:601-614.
13. Braff D., Stone C., Callaway E., Geyer M., Glick I., Bali L. Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 1978, 15:339-343.
14. Swerdlow N.R., Weber M., Qu Y., Light G.A., Braff D.L. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology 2008, 199:331-388.
15. Swerdlow N.R., Shilling P.D., Breier M., Trim R.S., Light G.A., Saint Marie R. Fronto-temporal-mesolimbic gene expression and heritable differences in amphetamine-disrupted sensorimotor gating in rats. Psychopharmacology 2012, 224:349-362.
16. Flores G., Alquicer G., Silva-Gómez A.B., Zaldivar G., Stewart J., Quirion R., Srivastava L.K. Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in post-pubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 2005, 133:463-470.
17. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002, 71:877-892.
18. Sobin C., Kiley-Brabeck K., Karayiorgou M. Lower prepulse inhibition in children with the 22q11 deletion syndrome. Am J Psychiatry 2005, 162:1090-1099.
19. Roussos P., Giakoumaki S.G., Rogdaki M., Pavlakis S., Frangou S., Bitsios P. Prepulse inhibition of the startle reflex depends on the catechol O-methyltransferase Val158Met gene polymorphism. Psychol Med 2008, 38:1651-1658.
20. Kao W.T., Wang Y., Kleinman J.E., Lipska B.K., Hyde T.M., Weinberger D.R., Law A.J. Common genetic variation in Neuregulin 3 (NRG3) influences risk for schizophrenia and impacts NRG3 expression in human brain. PNAS 2010, 107:15619-15624.
21. Quednow B.B., Wagner M., Mössner R., Maier W., Kuhn K.U. Sensorimotor gating of schizophrenia patients depends on catechol O-methyltransferase Val158Met polymorphism. Schizophr Bull 2010, 36:341-346.
22. Greenwood T.A., Lazzeroni L.C., Murray S.S., Cadenhead K.S., Calkins M.E., Dobie D.J., et al. Analysis of 94 candidate genes and twelve endophenotypes for schizophrenia from the consortium on the genetics of schizophrenia. Am J Psychiatry 2011, 168:930-946.
23. Greenwood T.A., Light G.A., Swerdlow N.R., Radant A.D., Braff D.L. Association analysis of 94 candidate genes and schizophrenia-related endophenotypes. PLoS Genet 2012, 7:e1002134.
24. Shilling P.D., Saint Marie R.L., Shoemaker J.M., Swerdlow N.R. Strain differences in the gating-disruptive effects of apomorphine: relationship to gene expression in nucleus accumbens signaling pathways. Biol Psychiatry 2008, 63:748-758.
25. Swerdlow N.R., Powell S.B., Breier M.R., Hines S.R., Light G.A. Coupling of gene expression in medial prefrontal cortex and nucleus accumbens after neonatal ventral hippocampal lesions accompanies deficits in sensorimotor gating and auditory processing in rats. Neuropharmacology 2013, 75C:38-46.
26. Swerdlow N.R., Shoemaker J.M., Crain S., Goins J., Onozuka K., Auerbach P.P. Sensitivity to drug effects on prepulse inhibition in inbred and outbred rat strains. Pharmacol Biochem Behav 2004, 77:291-302.
27. Bakshi V.P., Swerdlow N.R., Braff D.L., Geyer M.A. Reversal of isolation rearing-induced deficits in prepulse inhibition by Seroquel and olanzapine. Biol Psychiatry 1998, 43:436-445.
28. Harte M.K., Powell S.B., Swerdlow N.R., Geyer M.A., Reynolds G.P. Deficits in parvalbumin and calbindin immunoreactive cells in the hippocampus of isolation reared rats. J Neural Transm 2007, 114:893-898.
29. Bakshi V.P., Geyer M.A. Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats. Physiol Behav 1999, 67:385-392.
30. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego, CA. 4th ed.
31. Powell S.B., Swerdlow N.R., Pitcher L.K., Geyer M.A. Isolation rearing-induced deficits in prepulse inhibition and locomotor habituation are not potentiated by water deprivation. Physiol Behav 2002, 77:55-64.
32. Lehmann J., Pryce C.R., Feldon J. Sex differences in the acoustic startle response and prepulse inhibition in Wistar rats. Behav Brain Res 1999, 104:113-117.
33. Swerdlow N.R., Breier M., Mora A.B., Ko D., Shoemaker J.M. A novel rat strain with enhanced sensitivity to the effects of dopamine agonists on startle gating. Pharmacol Biochem Behav 2008, 88:280-290.
34. Bollen K.A. Structural equations with latent variables 1989, Wiley, New Jersey.
35. Muthén L.K., Muthén B.O. Mplus user's guide 1998-2011, Muthén & Muthén, Los Angeles, CA. 6th ed.
36. Cilia J., Hatcher P.D., Reavill C., Jones D.N. Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats: an update. Psychopharmacology 2005, 180:57-62.
37. Pietropaolo S., Singer P., Feldon J., Yee B.K. The postweaning social isolation in C57BL/6 mice: preferential vulnerability in the male sex. Psychopharmacology 2008, 197:613-628. 10.1007/s00213-008-1081-3.
38. Lim A.L., Taylor D.A., Malone D.T. Isolation rearing in rats: effect on expression of synaptic, myelin and GABA-related immunoreactivity and its utility for drug screening via the subchronic parenteral route. Brain Res 2011, 1381:52-65. 10.1016/j.brainres.2011.01.017.
39. Weiss I.C., Feldon J. Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 2001, 156:305-326.
40. Krebs-Thomson K., Giracello D., Solis A., Geyer M.A. Post-weaning handling attenuates isolation-rearing induced disruptions of prepulse inhibition in rats. Behav Brain Res 2001, 120:221-224.
41. Varty G.B., Higgins G.A. Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipsychotic drugs. Psychopharmacology 1995, 122:15-26.