Acute phencyclidine administration induces c-Fos-immunoreactivity in interneurons in cortical and subcortical regions

Neuroscience

Volumn 334, Issue , 2016, Pages 13-25

  Hervig, Mona E ^a,b   Thomsen, Morten S ^a,c   Kalló, Imre ^d   Mikkelsen, Jens D ^a  

^a University of Copenhagen   (Denmark)

^b BISPEBJERG HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

c Fos; interneurons; NMDA; phencyclidine; prefrontal cortex; schizophrenia

Indexed keywords

CALBINDIN; PARVALBUMIN; PHENCYCLIDINE; PROTEIN C FOS; 4 AMINOBUTYRIC ACID RECEPTOR; AMINO ACID RECEPTOR BLOCKING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFRALIMBIC CORTEX; INTERNEURON; MALE; MOTOR CORTEX; NONHUMAN; NUCLEUS ACCUMBENS; ORBITAL CORTEX; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; RETROSPLENIAL CORTEX; SOMATOSENSORY CORTEX; SUBCORTEX; THALAMUS; THALAMUS DORSOMEDIAL NUCLEUS; VENTROLATERAL ORBITAL CORTEX; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DRUG EFFECTS; METABOLISM; WISTAR RAT;

ANIMALS; BRAIN; CALBINDINS; EXCITATORY AMINO ACID ANTAGONISTS; GABAERGIC NEURONS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; PARVALBUMINS; PHENCYCLIDINE; PROTO-ONCOGENE PROTEINS C-FOS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84981719800     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.07.028     Document Type: Article

References (101)

1. Adler, C.M., Malhotra, A.K., Elman, I., Goldberg, T., Egan, M., Pickar, D., Breier, A., Comparison of ketamine-induced thought disorder in healthy volunteers and thought disorder in schizophrenia. Am J Psychiatry 156:10 (1999), 1646–1649.
2. Akbarian, S., Kim, J.J., Potkin, S.G., Hagman, J.O., Tafazzoli, A., Bunney, W.E., Jones, E.G., Gene expression for glutamic acid Is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52:4 (1995), 258–266.
3. Amargós-Bosch, M., López-Gil, X., Artigas, F., Adell, A., Clozapine and olanzapine, but not haloperidol, suppress serotonin efflux in the medial prefrontal cortex elicited by phencyclidine and ketamine. Int J Neuropsychopharmacol 9:5 (2006), 565–573.
4. Bakker, C.B., Amini, F.B., Observations on the psychotomimetic effects of Sernyl. Compr Psychiatry 2 (1961), 269–280.
5. Beasley, C.L., Reynolds, G.P., Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 24:3 (1997), 349–355.
6. Behrens, M.M., Ali, S.S., Dao, D.N., Lucero, J., Shekhtman, G., Quick, K.L., Dugan, L.L., Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318:5856 (2007), 1645–1647.
7. Belforte, J.E., Zsiros, V., Sklar, E.R., Jiang, Z., Yu, G., Li, Y., Quinlan, E.M., Nakazawa, K., Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 13:1 (2010), 76–83.
8. Berendse, H.W., Groenewegen, H.J., Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:1 (1991), 73–102.
9. Bluhm, R.L., Miller, J., Lanius, R.A., Osuch, E.A., Boksman, K., Neufeld, R.W., Théberge, J., Schaefer, B., Williamson, P.C., Retrosplenial cortex connectivity in schizophrenia. Psychiatry Res 174:1 (2009), 17–23.
10. Breier, A., Malhotra, A.K., Pinals, D.A., Weisenfeld, N.I., Pickar, D., Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers. Am J Psychiatry 154:6 (1997), 805–811.
11. Carlén, M., Meletis, K., Siegle, J.H., Cardin, J.A., Futai, K., Vierling-Claassen, D., Rühlmann, C., Jones, S.R., Deisseroth, K., Sheng, M., Moore, C.I., Tsai, L.H., A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17:5 (2012), 537–548.
12. Castañé, A., Santana, N., Artigas, F., PCP-based mice models of schizophrenia: differential behavioral, neurochemical and cellular effects of acute and subchronic treatments. Psychopharmacology, 232(21–22), 2015.
13. Castellani, S., Adams, P.M., Effects of dopaminergic drugs on phencyclidine-induced behaviour in the rat. Neuropharmacology 20 (1980), 371–374.
14. Celada, P., Lladó-Pelfort, L., Santana, N., Kargieman, L., Troyano-Rodriguez, E., Riga, M.S., Artigas, F., Disruption of thalamocortical activity in schizophrenia models: relevance to antipsychotic drug action. Int J Neuropsychopharmacol 16:10 (2013), 2145–2163.
15. Cenquizca, L.A., Swanson, L.W., Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1 (2007), 1–26.
16. Cho, R.Y., Konecky, R.O., Carter, C.S., Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci U S A 103:52 (2006), 19878–19883.
17. Cochran, S.M., Kennedy, M., McKerchar, C.E., Steward, L.J., Pratt, J.A., Morris, B.J., Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology 28:2 (2003), 265–275.
18. Danos, P., Baumann, B., Bernstein, H.G., Franz, M., Stauch, R., Northoff, G., Krell, D., Falkai, P., Bogerts, B., Schizophrenia and anteroventral thalamic nucleus: selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons. Psychiatry Res 82:1 (1998), 1–10.
19. De Leonibus, E., Mele, A., Oliverio, A., Pert, A., Distinct pattern of c-fos mRNA expression after systemic and intra-accumbens amphetamine and MK-801. Neuroscience 115:1 (2002), 67–78.
20. DeFelipe, J., Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1 (1997), 1–19.
21. Dietz, D.M., Kennedy, P.J., Sun, H., Maze, I., Gancarz, A.M., Vialou, V., Koo, J.W., Mouzon, E., Ghose, S., Tamminga, C.A., Nestler, E.J., ΔFosB induction in prefrontal cortex by antipsychotic drugs is associated with negative behavioral outcomes. Neuropsychopharmacology 39:3 (2014), 538–544.
22. Druga, R., Neocortical inhibitory system. Folia Biol (Praha) 217 (2009), 201–217.
23. Eyles, D.W., Mcgrath, J.J., Reynolds, G.P., Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 57:1 (2002), 27–34.
24. Fung, S.J., Webster, M.J., Sivagnanasundaram, S., Duncan, C., Elashoff, M., Weickert, C.S., Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry 167:12 (2010), 1479–1488.
25. Fung, S.J., Fillman, S.G., Webster, M.J., Shannon Weickert, C., Schizophrenia and bipolar disorder show both common and distinct changes in cortical interneuron markers. Schizophr Res 155:1–3 (2014), 26–30.
26. Fuster, J.M., The prefrontal cortex. 4th ed., 2008, Academic Press, London pp. 7–58.
27. Gao, X.M., Shirakawa, O., Du, F., Tamminga, C.A., Delayed regional metabolic actions of phencyclidine. Eur J Pharmacol 241:1 (1993), 7–15.
28. Gao, X.M., Hashimoto, T., Tamminga, C.A., Phencyclidine (PCP) and dizocilpine (MK801) exert time-dependent effects on the expression of immediate early genes in rat brain. Synapse 29:1 (1998), 14–28.
29. Gilmour, G., Dix, S., Fellini, L., Gastambide, F., Plath, N., Steckler, T., Talpos, J., Tricklebank, M., NMDA receptors, cognition and schizophrenia–testing the validity of the NMDA receptor hypofunction hypothesis. Neuropharmacology 62:3 (2012), 1401–1412.
30. Gonchar, Y., Burkhalter, A., Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:4 (1997), 347–358.
31. Gonzalez-Burgos, G., Lewis, D.A., NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia. Schizophr Bull 38:5 (2012), 950–957.
32. Gonzalez-Burgos, G., Cho, R.Y., Lewis, D.A., Alterations in cortical network oscillations and parvalbumin neurons in schizophrenia. Biol Psychiatry 77:12 (2015), 1031–1040.
33. Gotoh, L., Kawanami, N., Nakahara, T., Hondo, H., Motomura, K., Ohta, E., Kanchiku, I., Kuroki, T., Hirano, M., Uchimura, H., Effects of the adenosine A(1) receptor agonist N(6)-cyclopentyladenosine on phencyclidine-induced behavior and expression of the immediate-early genes in the discrete brain regions of rats. Brain Res Mol Brain Res 100:1–2 (2002), 1–12.
34. Griffiths, M.R., Mitchell, I.J., Cooper, A.J., Phencyclidine induces D-1 dopamine receptor mediated Fos-like immunoreactivity in discretely localised populations of striatopallidal and striatoentopeduncular neurons in the rat. Brain Res 821:1 (1999), 177–189.
35. Habara, T., Hamamura, T., Miki, M., Ohashi, K., Kuroda, S., M100907, a selective 5-HT(2A) receptor antagonist, attenuates phencyclidine-induced Fos expression in discrete regions of rat brain. Eur J Pharmacol 417:3 (2001), 189–194.
36. Haggerty, G.C., Forney, R.B., Johnson, J.M., The effect of a single administration of phencyclidine on behavior in the rat over a 21-day period. Toxicol Appl Pharmacol 75:3 (1984), 444–453.
37. Hashimoto, T., Volk, D.W., Eggan, S.M., Mirnics, K., Pierri, J.N., Sun, Z., Sampson, A.R., Lewis, D.A., Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23:15 (2003), 6315–6326.
38. Hashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J.G., Morris, H.M., Volk, D.W., Mirnics, K., Lewis, D.A., Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 13:2 (2008), 147–161.
39. Hashimoto, T., Bazmi, H.H., Mirnics, K., Wu, Q., Sampson, A.R., Lewis, D.A., Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry 165:4 (2008), 479–489.
40. Homayoun, H., Moghaddam, B., NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27:43 (2007), 11496–11500.
41. Iasevoli, F., Buonaguro, E.F., Sarappa, C., Marmo, F., Latte, G., Rossi, R., Eramo, A., Tomasetti, C., de Bartolomeis, A., Regulation of postsynaptic plasticity genes’ expression and topography by sustained dopamine perturbation and modulation by acute memantine: relevance to schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 3:54 (2014), 299–314.
42. Imre, G., Fokkema, D.S., Den Boer, J.A., Ter Horst, G.J., Dose-response characteristics of ketamine effect on locomotion, cognitive function and central neuronal activity. Brain Res Bull 69:3 (2006), 338–345.
43. Jackson, M.E., Homayoun, H., Moghaddam, B., NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci U S A 101:22 (2004), 8467–8472.
44. Javitt, D.C., Zukin, S.R., Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148:10 (1991), 1301–1308.
45. Javitt, D.C., Steinschneider, M., Schroeder, C.E., Arezzo, J.C., Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci U S A 93:21 (1996), 11962–11967.
46. Javitt, D.C., Zukin, S.R., Heresco-Levy, U., Umbricht, D., Has an angel shown the way? Etiological and therapeutic implications of the PCP/NMDA model of schizophrenia. Schizophr Bull 38:5 (2012), 958–966.
47. Jodo, E., The role of the hippocampo-prefrontal cortex system in phencyclidine-induced psychosis: a model for schizophrenia. J Physiol Paris 107:6 (2013), 434–440.
48. Jodo, E., Katayama, T., Okamoto, M., Suzuki, Y., Hoshino, K., Kayama, Y., Differences in responsiveness of mediodorsal thalamic and medial prefrontal cortical neurons to social interaction and systemically administered phencyclidine in rats. Neuroscience 170:4 (2010), 1153–1164.
49. Jodo, E., Suzuki, Y., Katayama, T., Hoshino, K.Y., Takeuchi, S., Niwa, S., Kayama, Y., Activation of medial prefrontal cortex by phencyclidine is mediated via a hippocampo-prefrontal pathway. Cereb Cortex 15:5 (2005), 663–669.
50. Jones, E.G., Hendry, S.H., Differential calcium-binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1:3 (1989), 222–246.
51. Kalinichev, M., Robbins, M.J., Hartfield, E.M., Maycox, P.R., Moore, S.H., Savage, K.M., Austin, N.E., Jones, D.N., Comparison between intraperitoneal and subcutaneous phencyclidine administration in Sprague–Dawley rats: a locomotor activity and gene induction study. Prog NeuroPsychopharmacol Biol Psychiatry 32:2 (2008), 414–422.
52. Kargieman, L., Santana, N., Mengod, G., Celada, P., Artigas, F., Antipsychotic drugs reverse the disruption in prefrontal cortex function produced by NMDA receptor blockade with phencyclidine. Proc Natl Acad Sci U S A 104:37 (2007), 14843–14848.
53. Kargieman, L., Santana, N., Mengod, G., Celada, P., Artigas, F., NMDA antagonist and antipsychotic actions in cortico-subcortical circuits. Neurotox Res 14:2–3 (2008), 129–140.
54. Kawaguchi, Y., Kubota, Y., GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:6 (1997), 476–486.
55. Kehrer, C., Maziashvili, N., Dugladze, T., Gloveli, T., Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci, 8(1), 2008, 6.
56. Keilhoff, G., Becker, A., Grecksch, G., Wolf, G., Bernstein, H.-G., Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 126:3 (2004), 591–598.
57. Kiss, T., Hoffmann, W.E., Scott, L., Kawabe, T.T., Milici, A.J., Nilsen, E.A., Hajós, M., Role of thalamic projection in NMDA receptor-induced disruption of cortical slow oscillation and short-term plasticity. Front Psychiatry, 4(2), 2011, 14.
58. Kolb, B., Pellis, S., Robinson, T.E., Plasticity and functions of the orbital frontal cortex. Brain Cogn 55:1 (2004), 104–115.
59. Korotkova, T., Fuchs, E.C., Ponomarenko, A., von Engelhardt, J., Monyer, H., NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68:3 (2010), 557–569.
60. Krystal, J.H., Karper, L.P., Seibyl, J.P., Freeman, G.K., Delaney, R., Bremner, J.D., Heninger, G.R., Bowers, M.B. Jr., Charney, D.S., Subanesthetic effects of the noncompetitive NMDA antagonist ketamine in humans Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:3 (1994), 199–214.
61. Lahti, A.C., Koffel, B., LaPorte, D., Tamminga, C.A., Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:1 (1995), 9–19.
62. Lewis, D.A., Cortical circuit dysfunction and cognitive deficits in schizophrenia–implications for preemptive interventions. Eur J Neurosci 35:12 (2012), 1871–1878.
63. Lewis, D.A., Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr Opin Neurobiol 26 (2014), 22–26.
64. Lewis, D.A., Hashimoto, T., Morris, H.M., Cell and receptor type-specific alterations in markers of GABA neurotransmission in the prefrontal cortex of subjects with schizophrenia. Neurotox Res 14:2–3 (2008), 237–248.
65. Lewis, D.A., Curley, A.A., Glausier, J.R., Volk, D.W., Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 35:1 (2012), 57–67.
66. Liposits, Z., Sétáló, G., Flerkó, B., Application of the silver-gold intensified 3,3′-diaminobenzidine chromogen to the light and electron microscopic detection of the luteinizing hormone-releasing hormone system of the rat brain. Neuroscience 13:2 (1984), 513–525.
67. López Hill, X., Scorza, M.C., Role of the anterior thalamic nucleus in the motor hyperactivity induced by systemic MK-801 administration in rats. Neuropharmacology 62:7 (2012), 2440–2446.
68. López-Gil, X., Babot, Z., Amargós-Bosch, M., Suñol, C., Artigas, F., Adell, A., Clozapine and haloperidol differently suppress the MK-801-increased glutamatergic and serotonergic transmission in the medial prefrontal cortex of the rat. Neuropsychopharmacology 32:10 (2007), 2087–2097.
69. Luby, E.D., Cohen, B.D., Rosenbaum, G., Gottlieb, J.S., Kelley, R., Study of a new schizomimetic drug – sernyl. AMA Arch Neurol Psychiatry 81:3 (1959), 363–369.
70. Malhotra, A.K., Adler, C.M., Kennison, S.D., Elman, I., Pickar, D., Breier, A., Clozapine blunts N-methyl-D-aspartate antagonist-induced psychosis: a study with ketamine. Biol Psychiatry 42:8 (1997), 664–668.
71. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., Wu, C., Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:10 (2004), 793–807.
72. McKibben, C.E., Jenkins, T.A., Adams, H.N., Harte, M.K., Reynolds, G.P., Effect of pretreatment with risperidone on phencyclidine-induced disruptions in object recognition memory and prefrontal cortex parvalbumin immunoreactivity in the rat. Behav Brain Res 208:1 (2010), 132–136.
73. Meltzer, H.Y., Massey, B.W., The role of serotonin receptors in the action of atypical antipsychotic drugs. Curr Opin Pharmacol 11:1 (2011), 59–67.
74. Meltzer, H.Y., Rajagopal, L., Huang, M., Oyamada, Y., Kwon, S., Horiguchi, M., Translating the N-methyl-D-aspartate receptor antagonist model of schizophrenia to treatments for cognitive impairment in schizophrenia. Int J Neuropsychopharmacol 16:10 (2013), 2181–2194.
75. Mikkelsen, J.D., Vrang, N., Mrosovsky, N., Expression of Fos in the circadian system following nonphotic stimulation. Brain Res Bull 47:4 (1998), 367–376.
76. Minzenberg, M.J., Laird, A.R., Thelen, S., Carter, C.S., Glahn, D.C., Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch Gen Psychiatry 66:8 (2009), 811–822.
77. Minzenberg, M.J., Firl, A.J., Yoon, J.H., Gomes, G.C., Reinking, C., Carter, C.S., Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology 35:13 (2010), 2590–2599.
78. Morris, B.J., Cochran, S.M., Pratt, J.A., PCP: from pharmacology to modelling schizophrenia. Curr Opin Pharmacol 5:1 (2005), 101–106.
79. Morrow, B.A., Elsworth, J.D., Roth, R.H., Repeated phencyclidine in monkeys results in loss of parvalbumin-containing axo-axonic projections in the prefrontal cortex. Psychopharmacology 192:2 (2007), 283–290.
80. Näkki, R., Sharp, F.R., Sagar, S.M., Honkaniemi, J., Effects of phencyclidine on immediate early gene expression in the brain. J Neurosci Res 45:1 (1996), 13–27.
81. Newcomer, J.W., Farber, N.B., Jevtovic-Todorovic, V., Selke, G., Melson, A.K., Hershey, T., Craft, S., Olney, J.W., Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 20:2 (1999), 106–118.
82. Paxinos, G., Watson, C., The rat brain in stereotaxic coordinates. 5th ed., 2004, Academic Press.
83. Price, J.L., Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann NY Acad Sci 1121 (2007), 54–71.
84. Purcell, S.M., Moran, J.L., Fromer, M., Ruderfer, D., Solovieff, N., Roussos, P., O'Dushlaine, C., Chambert, K., Bergen, S.E., Kähler, A., Duncan, L., Stahl, E., Genovese, G., Fernández, E., Collins, M.O., Komiyama, N.H., Choudhary, J.S., Magnusson, P.K., Banks, E., Shakir, K., Garimella, K., Fennell, T., DePristo, M., Grant, S.G., Haggarty, S.J., Gabriel, S., Scolnick, E.M., Lander, E.S., Hultman, C.M., Sullivan, P.F., McCarroll, S.A., Sklar, P., A polygenic burden of rare disruptive mutations in schizophrenia. Nature 506:7487 (2014), 185–190.
85. Rujescu, D., Bender, A., Keck, M., Hartmann, A.M., Ohl, F., Raeder, H., Giegling, I., Genius, J., McCarley, R.W., Möller, H.J., Grunze, H., A pharmacological model for psychosis based on N-methyl-D-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities. Biol Psychiatry 59:8 (2006), 721–729.
86. Sadikot, A.F., Sasseville, R., Neurogenesis in the mammalian neostriatum and nucleus accumbens: parvalbumin-immunoreactive GABAergic interneurons. J Comp Neurol 389:2 (1997), 193–211.
87. Santana, N., Troyano-Rodriguez, E., Mengod, G., Celada, P., Artigas, F., Activation of thalamocortical networks by the N-methyl-D-aspartate receptor antagonist phencyclidine: reversal by clozapine. Biol Psychiatry 69:10 (2011), 918–927.
88. Sato, D., Umino, A., Kaneda, K., Takigawa, M., Nishikawa, T., Developmental changes in distribution patterns of phencyclidine-induced c-Fos in rat forebrain. Neurosci Lett 239:1 (1997), 21–24.
89. Sohal, V.S., Zhang, F., Yizhar, O., Deisseroth, K., Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:7247 (2009), 698–702.
90. Suzuki, Y., Jodo, E., Takeuchi, S., Niwa, S., Kayama, Y., Acute administration of phencyclidine induces tonic activation of medial prefrontal cortex neurons in freely moving rats. Neuroscience 114:3 (2002), 769–779.
91. Tanaka, D.H., Toriumi, K., Kubo, K., Nabeshima, T., Nakajima, K.J., GABAergic precursor transplantation into the prefrontal cortex prevents phencyclidine-induced cognitive deficits. J Neurosci 31:40 (2011), 14116–14125.
92. Thomsen, M.S., Hansen, H.H., Mikkelsen, J.D., Opposite effect of phencyclidine on activity-regulated cytoskeleton-associated protein (Arc) in juvenile and adult limbic rat brain regions. Neurochem Int 56:2 (2010), 270–275.
93. Uhlhaas, P.J., Singer, W., Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:2 (2010), 100–113.
94. Väisänen, J., Ihalainen, J., Tanila, H., Castrén, E., Effects of NMDA-receptor antagonist treatment on c-fos expression in rat brain areas implicated in schizophrenia. Cell Mol Neurobiol 24:6 (2004), 769–780.
95. Van Groen, T., Wyss, J.M., Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:3 (2003), 249–263.
96. Volk, D.W., Austin, M.C., Pierri, J.N., Sampson, A.R., Lewis, D.A., Decreased glutamic acid decarboxylase 67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry 57:3 (2000), 237–245.
97. Vollenweider, F.X., Leenders, K.L., Scharfetter, C., Antonini, A., Maguire, P., Missimer, J., Angst, Metabolic hyperfrontality and psychopathology in the ketamine model of psychosis using positron emission tomography (PET) and [18F]fluorodeoxyglucose (FDG) J. Eur Neuropsychopharmacol 7:1 (1997), 9–24.
98. Woo, T.-U.W., Kim, A.M., Viscidi, E., Disease-specific alterations in glutamatergic neurotransmission on inhibitory interneurons in the prefrontal cortex in schizophrenia. Brain Res 1218 (2008), 267–277.
99. Zhang, Z.J., Reynolds, G.P., A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55:1–2 (2002), 1–10.
100. Zhang, Y., Llinas, R.R., Lisman, J.E., Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Front Neural Circ, 3, 2009, 20.
101. Zhang, Y., Yoshida, T., Katz, D.B., Lisman, J.E., NMDAR antagonist action in thalamus imposes δ oscillations on the hippocampus. J Neurophysiol 107:11 (2012), 3181–3189.