α4β2 nicotinic receptor stimulation of the GABAergic system within the orbitofrontal cortex ameliorates the severe crossmodal object recognition impairment in ketamine-treated rats: Implications for cognitive dysfunction in schizophrenia

Neuropharmacology

Volumn 90, Issue , 2015, Pages 42-52

  Cloke, Jacob M ^a   Winters, Boyer D ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Cross modal object recognition; GABA; Multisensory integration; Nicotinic receptors; NMDA receptor; Orbitofrontal cortex

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; KETAMINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2;

ANIMAL; DISEASE MODEL; DRUG EFFECTS; LONG EVANS RAT; MALE; METABOLISM; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; RANDOMIZATION; RECOGNITION; SCHIZOPHRENIA;

ANIMALS; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; KETAMINE; MALE; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; RANDOM ALLOCATION; RATS, LONG-EVANS; RECEPTORS, NICOTINIC; RECOGNITION (PSYCHOLOGY); SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 84914155969     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.11.004     Document Type: Article

References (102)

1. Z. Abdul-Monim, J.C. Neill, and G.P. Reynolds Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat J. Psychopharmacol. 21 2007 198 205
2. L. Adler, G. Rose, and R. Freedman Neurophysiological studies of sensory gating in rats: effects of amphetamine, phencyclidine, and haloperidol Biol. Psychiatry 21 1986 787 798
3. S. Akkerman, J. Prickaerts, H.W. Steinbusch, and A. Blokland Object recognition testing: statistical considerations Behav. Brain Res. 232 2012 317 322
4. E.X. Albuquerque, E.F.R. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
5. 2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus J. Neurophysiol. 86 2001 3043 3055
6. M. Alkondon, E.F. Pereira, H.M. Eisenberg, and E.X. Albuquerque Nicotinic receptor activation in human cerebral cortical interneurons: a mechanism for inhibition and disinhibition of neuronal networks J. Neurosci. 20 2000 66 75
7. P. Aracri, S. Consonni, R. Morini, M. Perrella, S. Rodighiero, A. Amadeo, and A. Becchetti Tonic modulation of GABA release by nicotinic acetylcholine receptors in layer V of the murine prefrontal cortex Cereb. Cortex 20 2010 1539 1555
8. S.J. Bartko, B.D. Winters, R.A. Cowell, L.M. Saksida, and T.J. Bussey Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations J. Neurosci. 27 2007 2548 2559
9. Beasley, and G. Reynolds Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics Schizophr. Res. 24 1997 349 355
10. Beasley, Z.J. Zhang, I. Patten, and G.P. Reynolds Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins Biol. Psychiatry 52 2002 708 715
11. M.M. Behrens, S.S. Ali, D.N. Dao, J. Lucero, G. Shekhtman, K.L. Quick, and L.L. Dugan Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase Science 318 2007 1645 1647
12. M. Bellani, S. Cerruti, P. Brambilla, M. Bellani, S. Cerruti, and P. Brambilla Orbitofrontal cortex abnormalities in schizophrenia Epidemiol. Psychiatric Sci. 19 2010 23 25
13. L. Braff Sensory input deficits and negative symptoms in schizophrenic patients Am. J. Psychiatry 126 1989 1006 1011
14. R.W. Buchanan, R.S. Keefe, J.A. Lieberman, D.M. Barch, J.G. Csernansky, D.C. Goff, J.M. Gold, M.F. Green, L.F. Jarskog, D.C. Javitt, D. Kimhy, M.S. Kraus, J.P. McEvoy, R.I. Mesholam-Gately, L.J. Seidman, M.P. Ball, R.P. McMahon, R.S. Kern, J. Robinson, and S.R. Marder A randomized clinical trial of MK-0777 for the treatment of cognitive impairments in people with schizophrenia Biol. Psychiatry 69 2011 442 449
15. P.D. Butler, S.M. Silverstein, and S.C. Dakin Visual perception and its impairment in schizophrenia Biol. Psychiatry 64 2008 40 47
16. M. Carlén, K. Meletis, J.H. Siegle, J.A. Cardin, K. Futai, D. Vierling-Claassen, C. Rühlmann, S.R. Jones, K. Deisseroth, M. Sheng, C.I. Moore, and L. Tsai A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior Mol. Psychiatry 17 2012 537 548
17. S.M. Cochran, M. Kennedy, C.E. McKerchar, L.J. Steward, J.A. Pratt, and B.J. Morris Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs Neuropsychopharmacology 28 2003 265 275
18. J. Courtin, F. Chaudun, R.R. Rozeske, N. Karalis, C. Gonzalez-Campo, H. Wurtz, A. Abdi, J. Baufreton, T.C. Bienvenu, and C. Herry Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression Nature 505 2014 92 96
19. T. Damgaard, N. Plath, J.C. Neill, and S.L. Hansen Extrasynaptic GABAA receptor activation reverses recognition memory deficits in an animal model of schizophrenia Psychopharmacology 214 2011 403 413
20. N. Dawson, X. Xiao, M. McDonald, D.J. Higham, B.J. Morris, and J.a Pratt Sustained NMDA receptor hypofunction induces compromised neural systems integration and schizophrenia-like alterations in functional brain networks Cereb. Cortex 24 2014 452 464
21. B. de Gelder, J. Vroomen, L. Annen, E. Masthof, and P. Hodiamont Audio-visual integration in schizophrenia Schizophr. Res. 59 2002 211 218
22. B. de Gelder, J. Vroomen, S.J. de Jong, E.D. Masthoff, F.J. Trompenaars, and P. Hodiamont Multisensory integration of emotional faces and voices in schizophrenics Schizophr. Res. 72 2004 195 203
23. J.J. de Jong, P.P.G. Hodiamont, and B. de Gelder Modality-specific attention and multisensory integration of emotions in schizophrenia: reduced regulatory effects Schizophr. Res. 122 2010 136 143
24. J.J. de Jong, P.P.G. Hodiamont, J. Van den Stock, and B. de Gelder Audiovisual emotion recognition in schizophrenia: reduced integration of facial and vocal affect Schizophr. Res. 107 2009 286 293
25. M.N.M. de Lima, D.C. Laranja, E. Bromberg, R. Roesler, and N. Schröder Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats Behav. Brain Res. 156 2005 139 143
26. S. Dix, and J.P. Aggleton Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition Behav. Brain Res. 99 1999 191 200
27. N. Durany, R. Zo, K.W. Boissl, and W. Paulus Human post-mortem striatal alpha4 beta2 nicotinic acetylcholine receptor density in schizophrenia and Parkinson's syndrome Neurosci. Lett. 287 2000 109 112
28. A. Ennaceur One-trial object recognition in rats and mice: methodological and theoretical issues Behav. Brain Res. 215 2010 244 254
29. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1988 47 59
30. J.M. Ford, M. Gray, S.L. Whitfield, U. Turken, and G. Glover Acquiring and inhibiting prepotent responses in schizophrenia Arch. Gen. Psychiatry 61 2004
31. R. Freedman, M. Hall, L. Adler, and S. Leonard Evidence in postmortem brain tisssue for decreased numbers of hippocampal nicotinic receptors in schizophrenia Biol. Psychiatry 38 1995 22 33
32. R. Freedman, A. Olincy, R.W. Buchanan, J. Harris, J. Gold, L. Johnson, D. Allensworth, A. Guzman-Bonilla, B. Clement, M.P. Ball, J. Kutnick, V. Pender, L. Martin, K. Stevens, B. Wagner, G. Zerbe, F. Soti, and W. Kem Initial phase 2 trial of a nicotinic agonist in schizophrenia Am. J. Psychiatry 165 2008 1040 1047
33. G. Gilmour, S. Dix, L. Fellini, F. Gastambide, N. Plath, T. Steckler, J. Talpos, and M. Tricklebank NMDA receptors, cognition and schizophrenia - testing the validity of the NMDA receptor hypofunction hypothesis Neuropharmacology 62 2012 1401 1412
34. B. Grayson, L. Adamson, M. Harte, M. Leger, S. Marsh, C. Piercy, and J.C. Neill The involvement of distraction in memory deficits induced by NMDAR antagonism: relevance to cognitive deficits in schizophrenia Behav. Brain Res. 2014 3 7
35. M.F. Green, R.S. Kern, and R.K. Heaton Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS Schizophr. Res. 72 2004 41 51
36. D.N. Harper An assessment and comparison of the effects of oxotremorine, D-cyloserine, and bicuculline on delayed matching-to-sample performance in rats Exp. Clin. Psychopharmacol. 8 2000 207 215
37. K. Hashimoto, T. Ishima, Y. Fujita, M. Matsuo, T. Kobashi, M. Takahagi, H. Tsukada, and M. Iyo Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of the novel selective alpha7 nicotinic receptor agonist SSR180711 Biol. Psychiatry 63 2008 92 97
38. T. Hauser, A. Kucinski, K. Jordan, G. Gatto, S. Wersinger, R. Hesse, E. Stachowiak, M. Stachowiak, R. Papker, P. Lippiello, and M. Bencherif TC-5619: an alpha7 neuronal nicotinic receptor-selective agonist that demonstrates efficacy in animal models of the positive and negative symptoms and cognitive dysfunction of schizophrenia Biochem. Pharmacol. 78 2010 803 812
39. E.L. Hindley, A.J. Nelson, J.P. Aggleton, and S.D. Vann Dysgranular retrosplenial cortex lesions in rats disrupt cross-modal object recognition Learn. Mem. 21 2014 171 179
40. H. Homayoun, and B. Moghaddam Orbitofrontal cortex neurons as a common target for classic and glutamatergic antipsychotic drugs Proc. Natl. Acad. Sci. U. S. A. 105 2008 18041 18046
41. L.E. Hong, G.K. Thaker, R.P. McMahon, A. Summerfelt, J. Rachbeisel, R.L. Fuller, I. Wonodi, R.W. Buchanan, C. Myers, S.J. Heishman, J. Yang, and A. Nye Effects of moderate-dose treatment with varenicline on neurobiological and cognitive biomarkers in smokers and nonsmokers with schizophrenia or schizoaffective disorder Arch. Gen. Psychiatry 68 2011 1195 1206
42. T. Itil, A. Keskiner, N. Kiremitci, and J. Holden Effect of phencyclidine in chronic schizophrenics Can. J. Psychiatry 12 1967 209 212
43. D.L. Jacklin, A. Goel, K.J. Clementino, A.W.M. Hall, J.C. Talpos, and B.D. Winters Severe cross-modal object recognition deficits in rats treated sub-chronically with NMDA receptor antagonists are reversed by systemic nicotine: implications for abnormal multisensory integration in schizophrenia Neuropsychopharmacology 37 2012 2322 2331
44. J.D. Jentsch, and R.H. Roth The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia Neuropsychopharmacology 20 1999 201 225
45. C.K. Jones, N. Byun, and M. Bubser Muscarinic and nicotinic acetylcholine receptor agonists and allosteric modulators for the treatment of schizophrenia Neuropsychopharmacology 37 2012 16 42
46. N. Kanahara, Y. Sekine, T. Haraguchi, Y. Uchida, K. Hashimoto, E. Shimizu, and M. Iyo Orbitofrontal cortex abnormality and deficit schizophrenia Schizophr. Res. 143 2013 246 252
47. S. Karamihalev, J. Prickaerts, and N.P. van Goethem Donepezil and the alpha-7 agonist PHA 568487, but not risperidone, ameliorate spatial memory deficits in a subchronic MK-801 mouse model of cognitive impairment in schizophrenia Behav. Brain Res. 272 2014 248 251
48. G. Keilhoff, A. Becker, G. Grecksch, G. Wolf, and H.-G. Bernstein 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 126 2004 591 598
49. T. Korotkova, E.C. Fuchs, A. Ponomarenko, J. von Engelhardt, and H. Monyer NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory Neuron 68 2010 557 569
50. J.H. Krystal, L.P. Karper, J.P. Seibyl, G.K. Freeman, R. Delaney, D. Bremner, G.R. Heninger, M.B. Bowers Jr., and D.S. Charney Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans Arch. Gen. Psychiatry 51 1994 199 214
51. E.D. Levin, F.J. McClernon, and A.H. Rezvani Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization Psychopharmacology 184 2006 523 539
52. D.A. Lewis, R.Y. Cho, C.S. Carter, K. Eklund, S. Forster, M. Kelly, and D. Montrose Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia Am. J. Psychiatry 165 2008 1585 1593
53. D.A. Lewis, A.A. Curley, J.R. Glausier, and D.W. Volk Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia Trends Neurosci. 35 2012 57 67
54. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat. Rev. Neurosci. 6 2005 312 324
55. J.A. Lieberman, G. Dunbar, A.C. Segreti, R.R. Girgis, F. Seoane, J.S. Beaver, N. Duan, and D.A. Hosford A randomized exploratory trial of an alpha-7 nicotinic receptor agonist (TC-5619) for cognitive enhancement in schizophrenia Neuropsychopharmacology 38 2013 968 975
56. D.J. Lodge, M.M. Behrens, and A.A. Grace A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia J. Neurosci. 29 2009 2344 2354
57. E. Luby, B. Cohen, G. Rosenbaum, J. Gottieb, and R. Kelley Study of a new schizophrenomimetic drug; sernyl Arch. Neurol. Psychiatry 81 1959 363 369
58. L. Lyon, L.M. Saksida, and T.J. Bussey Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models Psychopharmacology 220 2012 647 672
59. E. Maloku, B. Kadriu, A. Zhubi, E. Dong, F. Pibiri, R. Satta, and A. Guidotti Selective alpha4beta2 nicotinic acetylcholine receptor agonists target epigenetic mechanisms in cortical GABAergic neurons Neuropsychopharmacology 36 2011 1366 1374
60. A.M. Melichercik, K.S. Elliott, C. Bianchi, S.M. Ernst, and B.D. Winters Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats Neuropharmacology 62 2012 2096 2105
61. L. Menzies, C. Ooi, S. Kamath, J. Suckling, P. McKenna, P. Fletcher, E.T. Bullmore, and C. Stephenson Effects of gamma-aminobutyric acid-modulating drugs on working memory and brain function in patients with schizophrenia Arch. Gen. Psychiatry 64 2007
62. J.C. Neill, S. Barnes, S. Cook, B. Grayson, N.F. Idris, S.L. McLean, S. Snigdha, L. Rajagopal, and M.K. Harte Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism Pharmacol. Ther. 128 2010 419 432
63. K.H. Nuechterlein, D.M. Barch, J.M. Gold, T.E. Goldberg, M.F. Green, and R.K. Heaton Identification of separable cognitive factors in schizophrenia Schizophr. Res. 72 2004 29 39
64. U. Olcese, G. Iurilli, and P. Medini Cellular and synaptic architecture of multisensory integration in the mouse neocortex Neuron 79 2013 579 593
65. A. Olincy, J. Harris, L. Johnson, V. Pender, S. Kongs, D. Allensworth, J. Ellis, G. Zerbe, S. Leonard, S. Stevens, K. Stevens, J. Stevnes, L. Martin, L. Adler, F. Soti, W.R. Kem, and R. Freedman Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia Arch. Gen. Psychiatry 63 2006 630 638
66. J.W. Olney, J.W. Newcomer, and N.B. Farber NMDA receptor hypofunction model of schizophrenia J. Psychiatric Res. 33 1999 523 533
67. D. Pearl, D. Yodashkin-Porat, N. Katz, A. Valevski, D. Aizenberg, M. Sigler, A. Weizman, and L. Kikinzon Differences in audiovisual integration, as measured by McGurk phenomenon, among adult and adolescent patients with schizophrenia and age-matched healthy control groups Compr. Psychiatry 50 2009 186 192
68. P. Pichat, O.E. Bergis, J.-P. Terranova, A. Urani, C. Duarte, V. Santucci, C. Gueudet, C. Voltz, R. Steinberg, J. Stemmelin, F. Oury-Donat, P. Avenet, G. Griebel, and B. Scatton SSR180711, a novel selective alpha7 nicotinic receptor partial agonist: (II) efficacy in experimental models predictive of activity against cognitive symptoms of schizophrenia Neuropsychopharmacology 32 2007 17 34
69. J.A. Pratt, C. Winchester, A. Egerton, S.M. Cochran, and B.J. Morris Modelling prefrontal cortex deficits in schizophrenia: implications for treatment Br. J. Pharmacol. 153 Suppl. l 2008 S465 S470
70. K.A. Radcliffe, J.L. Fisher, R. Gray, and J.A. Dani Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons Ann. N. Y. Acad. Sci. 868 1999 591 610
71. R.J. Radek, K.L. Kohlhaas, L. Rueter, and E. Mohler Treating cognitive deficits of schizophrenia with alpha4beta2 neuronal nicotinic receptor agonists Curr. Pharm. Des. 16 2010 309 322
72. R.J. Radek, H.M. Miner, N.A. Bratcher, M.W. Decker, M. Gopalakrishnan, and R.S. Bitner Alpha4beta2 nicotinic receptor stimulation contributes to the effects of nicotine in the DBA/2 mouse model of sensory gating Psychopharmacology 187 2006 47 55
73. J.M. Reid, D.L. Jacklin, and B.D. Winters Crossmodal object recognition in rats with and without multimodal object pre-exposure: no effect of hippocampal lesions Neurobiol. Learn. Mem. 98 2012 311 319
74. J.M. Reid, D.L. Jacklin, and B.D. Winters Delineating prefrontal cortex region contributions to crossmodal object recognition in rats Cereb. Cortex 24 2013 2108 2119
75. T. Romon, G. Mengod, and A. Adell Expression of parvalbumin and glutamic acid decarboxylase-67 after acute administration of MK-801. Implications for the NMDA hypofunction model of schizophrenia Psychopharmacology 217 2011 231 238
76. L.A. Ross, D. Saint-Amour, V.M. Leavitt, S. Molholm, D.C. Javitt, and J.J. Foxe Impaired multisensory processing in schizophrenia: deficits in the visual enhancement of speech comprehension under noisy environmental conditions Schizophr. Res. 97 2007 173 183
77. S.L. Rushforth, T. Steckler, and M. Shoaib Nicotine improves working memory span capacity in rats following sub-chronic ketamine exposure Neuropsychopharmacology 36 2011 2774 2781
78. J.J. Sabbagh, A.S. Murtishaw, M.M. Bolton, C.F. Heaney, M. Langhardt, and J.W. Kinney Chronic ketamine produces altered distribution of parvalbumin-positive cells in the hippocampus of adult rats Neurosci. Lett. 550 2013 69 74
79. D. Senkowski, T.R. Schneider, J.J. Foxe, and A.K. Engel Crossmodal binding through neural coherence: implications for multisensory processing Trends Neurosci. 31 2008 401 409
80. J.C. Shim, D.U. Jung, S.S. Jung, Y.S. Seo, D.M. Cho, J.H. Lee, S.W. Lee, B.G. Kong, J.W. Kang, M.K. Oh, S.D. Kim, R.P. McMahon, and D.L. Kelly Adjunctive varenicline treatment with antipsychotic medications for cognitive impairments in people with schizophrenia: a randomized double-blind placebo-controlled trial Neuropsychopharmacology 37 2012 660 668
81. R.C. Smith, J.P. Lindenmayer, J.M. Davis, J. Cornwell, K. Noth, S. Gupta, H. Sershen, and A. Lajtha Cognitive and antismoking effects of varenicline in patients with schizophrenia or schizoaffective disorder Schizophr. Res. 110 2009 149 155
82. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
83. J.J. Stekelenburg, J.P. Maes, A.R. Van Gool, M. Sitskoorn, and J. Vroomen Deficient multisensory integration in schizophrenia: an event-related potential study Schizophr. Res. 147 2013 253 261
84. D.B. Stone, L.J. Urrea, C.J. Aine, J.R. Bustillo, V.P. Clark, and J.M. Stephen Unisensory processing and multisensory integration in schizophrenia: a high-density electrical mapping study Neuropsychologia 49 2011 3178 3187
85. M.S. Thomsen, D.Z. Christensen, H.H. Hansen, J.P. Redrobe, and J.D. Mikkelsen alpha(7) Nicotinic acetylcholine receptor activation prevents behavioral and molecular changes induced by repeated phencyclidine treatment Neuropharmacology 56 2009 1001 1009
86. D.B. Timmermann, J.H. Grønlien, K.L. Kohlhaas, E.∅. Nielsen, E. Dam, T.D. Jørgensen, P.K. Ahring, D. Peters, D. Holst, J.K. Chrsitensen, J. Malysz, C.A. Briggs, M. Gopalakrishnan, and G.M. Olsen An allosteric modulator of the alpha 7 nicotinic acetylcholine receptor possessing cognition-enhancing properties in vivo J. Pharmacol. Exp. Ther. 323 2009 294 307
87. O.A. Timofeeva, and E.D. Levin Glutamate and nicotinic receptor interactions in working memory: importance for the cognitive impairment of schizophrenia Neuroscience 195 2011 21 36
88. P.J. Uhlhaas, and W. Singer Abnormal neural oscillations and synchrony in schizophrenia Nat. Rev. Neurosci. 11 2010 100 113
89. D. Umbricht, R.S. Keefe, S. Murray, D.A. Lowe, R. Porter, G. Garibaldi, and L. Santarelli A randomized, placebo-controlled study investigating the nicotinic alpha7 agonist, RG3487, for cognitive deficits in schizophrenia Neuropsychopharmacology 39 2014 1568 1577
90. A. Vaicelinunaite, S. Erisken, F. Franzen, S. Katzner, and L. Busse Spatial integration in mouse primary visual cortex J. Physiol. 110 2013 964 972
91. D. Velligan, R. Brenner, F. Sicuro, D. Walling, R. Riesenberg, A. Sfera, C. Merideth, D. Sweitzer, and J. Jaeger Assessment of the effects of AZD3480 on cognitive function in patients with schizophrenia Schizophr. Res. 134 2012 59 64
92. M.C. Waldo, L. Woodward, and L.E. Adler Varenicline and P50 auditory gating in medicated schizophrenic patients: a pilot study Psychiatry Res. 175 2010 179 180
93. T.L. Wallace, P.M. Callahan, A. Tehim, D. Bertrand, G. Tombaugh, S. Wang, W. Xie, W.B. Rowe, V. Ong, E. Graham, A.V. Terry, J.S. Rodefer, B. Herbert, M. Murray, R. Porter, L. Santarelli, and D.A. Lowe RG3487, a novel nicotinic alpha7 receptor partial agonist, improves cognition and sensorimotor gating in rodents J. Pharmacol. Exp. Ther. 336 2011 242 253
94. K.M. Wildeboer, and K.E. Stevens Stimulation of the alpha4beta2 nicotinic receptor by 5-I A-85380 improves auditory gating in DBA/2 mice Brain Res. 1224 2008 29 36
95. L.E. Williams, G.A. Light, D.L. Braff, and V.S. Ramachandran Reduced multisensory integration in patients with schizophrenia on a target detection task Neuropsychologia 48 2010 3128 3136
96. B.D. Winters, S.E. Forwood, R.A. Cowell, L.M. Saksida, and T.J. Bussey Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe J. Neurosci. 24 2004 5901 5908
97. B.D. Winters, and J.M. Reid A distributed cortical representation underlies crossmodal object recognition in rats J. Neurosci. 30 2010 6253 6261
98. J. Wood, Y. Kim, and B. Moghaddam Disruption of prefrontal cortex large scale neuronal activity by different classes of psychotomimetic drugs J. Neurosci. 32 2012 3022 3031
99. J.W. Young, S. Powell, V. Risbrough, H.M. Marston, and A. Mark Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia Pharmacol. Ther. 122 2009 150 202
100. X. Zhang, L. Liu, S. Liu, X. Hong, D. Chen, M. Xiu, F. Yang, Z. Zhang, X. Zhang, T. Kosten, and T. Kosten Short-term tropisetron treatment and cognitive and p50 auditory gating deficits in schizophrenia Am. J. Psychiatry 169 2012 974 981
101. Z. Zhang, and G.P. Reynolds A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia Schizophr. Res. 55 2002 1 10
102. M. Zvyagintsev, C. Parisi, N. Chechko, A.R. Nikolaev, and K. Mathiak Attention and multisensory integration of emotions in schizophrenia Front. Hum. Neurosci. 7 2013 674