Prenatal immune activation alters hippocampal place cell firing characteristics in adult animals

Brain, Behavior, and Immunity

Volumn 48, Issue , 2015, Pages 232-243

  Wolff, Amy R ^a   Bilkey, David K ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Autism; Bipolar; Hippocampus; Maternal; Memory; Place cell; Poly I:C; Rat; Schizophrenia; Synchrony

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DAM (ANIMAL); ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; FEMALE; FIRING RATE; GAMMA RHYTHM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; IMMUNOREACTIVITY; INFANT; LOCAL FIELD POTENTIAL; MALE; MATERNAL IMMUNE ACTIVATION; NONHUMAN; PLACE CELL; PRIORITY JOURNAL; PROGENY; PYRAMIDAL NERVE CELL; RAT; WAVEFORM; ACTION POTENTIAL; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HIPPOCAMPUS; IMMUNOLOGY; NERVE CELL; PREGNANCY; PRENATAL EXPOSURE;

POLYINOSINIC POLYCYTIDYLIC ACID;

ACTION POTENTIALS; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; MALE; NEURONS; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

EID: 84942991188     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.03.012     Document Type: Article

References (125)

1. Aleman, A., Hijman, R., de Haan, E.H., Kahn, R.S., 1999. Memory impairment in schizophrenia: a meta-analysis. Am. J. Psychiatry 156, 1358-1366.
2. Alme, C., Miao, C., Jezek, K., Treves, A., Moser, E., Moser, M., 2014. Place cells in the hippocampus: eleven maps for eleven rooms. Proc. Natl. Acad. Sci. U.S.A. 111, 18428-18435.
3. Altshuler, L.L., Casanova, M.F., Goldberg, T.E., Kleinman, J.E., 1990. The hippocampus and parahippocampus in schizophrenia, suicide, and control brains. Arch. Gen. Psychiatry 47, 1029-1034.
4. Atladóttir, H.Ó., Henriksen, T.B., Schendel, D.E., Parner, E.T., 2012. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics 130, e1447-e1454.
5. Atladóttir, H.O., Thorsen, P., Østergaard, L., Schendel, D.E., Lemcke, S., Abdallah, M., Parner, E.T., 2010. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J. Autism Dev. Disord. 40, 1423-1430.
6. Aylward, E., Minshew, N., Goldstein, G., Honeycutt, N., Augustine, A., Yates, K., Barta, P., Pearlson, G., 1999. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 53, 2145-2150.
7. Bauman, M., Losif, A., Smith, S., Bregere, C., Amaral, D., Patterson, P., 2014. Activation of the maternal immune system during pregnancy alters behavioral development of rhesus monkey offspring. Biol. Psychiatry 75, 332-341.
8. Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P., Gioanni, Y., Battaglia, F., Wiener, S., 2010. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66, 921-936.
9. Bi, G., Poo, M., 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464-10472.
10. Bilkey, D., 2014. Hippocampal activity in adult animals following maternal immune activation, a risk factor for schizophrenia. In: Matariki Network Conference: Brain and Mind Integrative Neuroscience, Dunedin, New Zealand.
11. Bilkey, D., Muir, G., 1999. A low cost, high precision subminiature microdrive for extracellular unit recording in behaving animals. J. Neurosci. Methods 92, 87-90.
12. Bilkey, D., Russell, N., Colombo, M., 2003. A lightweight microdrive for single-unit recording in freely moving rats and pigeons. Methods 30, 152-158.
13. Bitanihirwe, B.K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., Meyer, U., 2010a. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 35, 2462-2478.
14. Bitanihirwe, B.K., Weber, L., Feldon, J., Meyer, U., 2010b. Cognitive impairment following prenatal immune challenge in mice correlates with prefrontal cortical AKT1 deficiency. Int. J. Neuropsychopharmacol., 1-16
15. Boronat, S., Mehan, W., Shaaya, E., Thibert, R., Caruso, P., 2014. Hippocampal abnormalities in magnetic resonance imaging (MRI) of 15q duplication syndromes. J. Child Neurol., Epub Ahead of Print
16. Bose, A., Recce, M., 2001. Phase precession and phase-locking of hippocampal pyramidal cells. Hippocampus 11, 204-215.
17. Boucher, J., Mayes, A., Bigham, S., 2012. Memory in autistic spectrum disorder. Psychol. Bull. 138, 458-496.
18. Brankack, J., Stewart, M., Fox, S., 1993. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res. 615, 310-327.
19. Brown, A., 2012. Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev. Neurobiol. 72, 1272-1276.
20. Brown, A., Derkits, E., 2010. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 167, 261-280.
21. Brown, A., Susser, E., 2002. In utero infection and adult schizophrenia. Ment. Retard. Dev. Disabil. Res. Rev. 8, 51-57.
22. Browning, M.D., Dudek, E.M., Rapier, J.L., Leonard, S., Freedman, R., 1993. Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics. Biol. Psychiatry 34, 529-535.
23. Burwell, R., Amaral, D., 1998. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J. Comp. Neurol. 398, 179-205.
24. Buzsaki, G., 2002. Theta oscillations in the hippocampus. Neuron 33, 325-340.
25. Buzsáki, G., Rappelsberger, P., Kellényi, L., 1985. Depth profiles of hippocampal rhythmic slow activity ('theta rhythm') depend on behaviour. Electroencephalogr. Clin. Neurophysiol. 61, 77-88.
26. Clare, L., McKenna, P., Mortimer, A., Baddeley, A., 1993. Memory in schizophrenia: what is impaired and what is preserved? Neuropsychologia 31, 1225-1241.
27. Cohen, J.D., Barch, D.M., Carter, C., Servan-Schreiber, D., 1999. Context-processing deficits in schizophrenia: converging evidence from three theoretically motivated cognitive tasks. J. Abnorm. Psychol. 108, 120-133.
28. Cohen, J.D., Braver, T.S., O'Reilly, R.C., 1996. A computational approach to prefrontal cortex, cognitive control and schizophrenia: recent developments and current challenges. Philos. Trans. R. Soc. Lond. 351, 1515-1527.
29. Courchesne, E., Mouton, P., Calhoun, M., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M., Barnes, C., Pierce, K., 2011. Neuron number and size in prefrontal cortex of children with autism. JAMA 306, 2001-2010.
30. Csernansky, J.G., Joshi, S., Wang, L., Haller, J.W., Gado, M., Miller, J.P., Grenander, U., Miller, M.I., 1998. Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proc. Natl. Acad. Sci. U.S.A. 95, 11406-11411.
31. Csernansky, J.G., Wang, L., Jones, D., Rastogi-Cruz, D., Posener, J.A., Heydebrand, G., Miller, J.P., Miller, M.I., 2002. Hippocampal deformities in schizophrenia characterized by high dimensional brain mapping. Am. J. Psychiatry 159, 2000-2006.
32. Di Prisco, G., Vertes, R., 2006. Excitatory actions of the ventral midline thalamus (rhomboid/reuniens) on the medial prefrontal cortex in the rat. Synapse (New York, NY) 60, 45-55.
33. Dickerson, D., Overeem, K., Wolff, A., Williams, J., Abraham, W., Bilkey, D., 2014. Association of aberrant neural synchrony and altered GAD67 expression following exposure to maternal immune activation, a risk factor for schizophrenia. Transl. Psychiatry 4, e418.
34. Dickerson, D.D., Wolff, A.R., Bilkey, D.K., 2010. Abnormal long-range neural synchrony in a maternal immune activation animal model of schizophrenia. J. Neurosci. 30, 12424-12431.
35. Eastwood, S.L., Burnet, P.W., Harrison, P.J., 1995. Altered synaptophysin expression as a marker of synaptic pathology in schizophrenia. Neuroscience 66, 309-319.
36. Eastwood, S.L., Harrison, P.J., 2000. Hippocampal synaptic pathology in schizophrenia, bipolar disorder and major depression: a study of complexin mRNAs. Mol. Psychiatry 5, 425-432.
37. Ekstrom, A.D., Kahana, M.J., Caplan, J.B., Fields, T.A., Isham, E.A., Newman, E.L., Fried, I., 2003. Cellular networks underlying human spatial navigation. Nature 425, 184-188.
38. Fajnerová, I., Rodriguez, M., Levčík, D., Konrádová, L., Mikoláš, P., Brom, C., Stuchlík, A., Vlček, K., Horáček, J., 2014. A virtual reality task based on animal research - spatial learning and memory in patients after the first episode of schizophrenia. Front. Behav. Neurosci. 8, 157.
39. Fruntes, V., Limosin, F., 2008. Schizophrenia and viral infection during neurodevelopment: a pathogenesis model? Med. Sci. Monit. 14, 71-77.
40. Fyhn, M., Hafting, T., Treves, A., Moser, M.B., Moser, E.I., 2007. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190-194.
41. Gallagher, P., Gray, J., Kessels, R., 2014. Fractionation of visuo-spatial memory processes in bipolar depression: a cognitive scaffolding account. Psychol. Med. 17, 1-14.
42. Gandal, M., Nesbitt, A., McCurdy, R., Alter, M., 2012. Measuring the maturity of the fast-spiking interneuron transcriptional program in autism, schizophrenia, and bipolar disorder. PLoS One 7, e41215.
43. Gaskin, S., Gamliel, A., Tardif, M., Cole, E., Mumby, D.G., 2009. Incidental (unreinforced) and reinforced spatial learning in rats with ventral and dorsal lesions of the hippocampus. Behav. Brain Res. 202, 64-70.
44. Giovanoli, S., Meyer, U., 2013. Response to comment on "Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice". Science (New York, NY) 340
45. Giovanoli, S., Weber, L., Meyer, U., 2014. Single and combined effects of prenatal immune activation and peripubertal stress on parvalbumin and reelin expression in the hippocampal formation. Brain Behav. Immun. 40, 48-54.
46. Guidotti, A., Auta, J., Davis, J.M., Di-Giorgi-Gerevini, V., Dwivedi, Y., Grayson, D.R., Impagnatiello, F., Pandey, G., Pesold, C., Sharma, R., Uzunov, D., Costa, E., 2000. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch. Gen. Psychiatry 57, 1061-1069.
47. Hasselmo, M., Stern, C., 2014. Theta rhythm and the encoding and retrieval of space and time. NeuroImage 85, 656-666.
48. Haukvik, U., Westlye, L., Mørch-Johnsen, L., Jørgensen, K., Lange, E., Dale, A., Melle, I., Andreassen, O., Agartz, I., 2014. In vivo hippocampal subfield volumes in schizophrenia and bipolar disorder. Biol. Psychiatry, Epub Ahead of Print.
49. Howard, L., Kumaran, D., Ólafsdóttir, H., Spiers, H., 2011. Double dissociation between hippocampal and parahippocampal responses to object-background context and scene novelty. J. Neurosci. 31, 5253-5261.
50. Huxter, J., Burgess, N., O'Keefe, J., 2003. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828-832.
51. Ibi, D., Nagai, T., Kitahara, Y., Mizoguchi, H., Koike, H., Shiraki, A., Takuma, K., Kamei, H., Noda, Y., Nitta, A., Nabeshima, T., Yoneda, Y., Yamada, K., 2009. Neonatal polyI:C treatment in mice results in schizophrenia-like behavioral and neurochemical abnormalities in adulthood. Neurosci. Res. 64, 297-305.
52. Isaac, J.T., Buchanan, K.A., Muller, R.U., Mellor, J.R., 2009. Hippocampal place cell firing patterns can induce long-term synaptic plasticity in vitro. J. Neurosci. 29, 6840-6850.
53. Ito, H.T., Smith, S.E., Hsiao, E., Patterson, P.H., 2010. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav. Immun. 24, 930-941.
54. Jacot-Descombes, S., Uppal, N., Wicinski, B., Santos, M., Schmeidler, J., Giannakopoulos, P., Heinsen, H., Schmitz, C., Hof, P., 2012. Decreased pyramidal neuron size in brodmann areas 44 and 45 in patients with autism. Acta Neuropathol. 124, 67-79.
55. Jeffery, K.J., Anderson, M.I., 2003. Dissociation of the geometric and contextual influences on place cells. Hippocampus 13, 868-872.
56. Jensen, O., Lisman, J.E., 2000. Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J. Neurophysiol. 83, 2602-2609.
57. Jung, M.W., Wiener, S.I., McNaughton, B.L., 1994. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356.
58. Kjelstrup, K.B., Solstad, T., Brun, V.H., Hafting, T., Leutgeb, S., Witter, M.P., Moser, E.I., Moser, M.B., 2008. Finite scale of spatial representation in the hippocampus. Science (New York, NY) 321, 140-143.
59. Knierim, J., Hamilton, D., 2011. Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol. Rev. 91, 1245-1279.
60. Knuesel, I., Chicha, L., Britschgi, M., Schobel, S., Bodmer, M., Hellings, J., Toovey, S., Prinssen, E., 2014. Maternal immune activation and abnormal brain development across CNS disorders. Nat. Rev. Neurol. 10, 643-660.
61. Kopald, B., Mirra, K., Egan, M., Weinberger, D., Goldberg, T., 2012. Magnitude of impact of executive functioning and IQ on episodic memory in Schizophrenia. Biol. Psychiatry 71, 545-551.
62. Kubie, J., Muller, R., Bostock, E., 1990. Spatial firing properties of hippocampal theta cells. J. Neurosci. 10, 1110-1123.
63. Kyd, R.J., Bilkey, D.K., 2003. Prefrontal cortex lesions modify the spatial properties of hippocampal place cells. Cereb. Cortex 13, 444-451.
64. Kyd, R.J., Bilkey, D.K., 2005. Hippocampal place cells show increased sensitivity to changes in the local environment following prefrontal cortex lesions. Cereb. Cortex 15, 720-731.
65. Lazic, S., 2013. Comment on "Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice". Science (New York, NY) 340.
66. Ledoux, A., Boyer, P., Phillips, J., Labelle, A., Smith, A., Bohbot, V., 2014. Structural hippocampal anomalies in a schizophrenia population correlate with navigation performance on a wayfinding task. Front. Behav. Neurosci. 14, 8-88.
67. Lenck-Santini, P.P., Save, E., Poucet, B., 2001. Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 11, 377-390.
68. Leutgeb, S., Leutgeb, J.K., Barnes, C.A., Moser, E.I., McNaughton, B.L., Moser, M.B., 2005. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science (New York, NY) 309, 619-623.
69. Lever, C., Wills, T., Cacucci, F., Burgess, N., O'Keefe, J., 2002. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90-94.
70. Levy, W., Steward, O., 1983. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8, 791-797.
71. Lewis, D., Fish, K., Arion, D., Gonzalez-Burgos, G., 2011. Perisomatic inhibition and cortical circuit dysfunction in schizophrenia. Curr. Opin. Neurobiol. 21, 866-872.
72. Lind, S., Williams, D., Raber, J., Peel, A., Bowler, D., 2013. Spatial navigation impairments among intellectually high-functioning adults with autism spectrum disorder: exploring relations with theory of mind, episodic memory, and episodic future thinking. J. Abnorm. Psychol. 122, 1189-1199.
73. Lisman, J.E., Buzsáki, G., 2008. A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr. Bull. 34, 974-980.
74. Lu, X., Bilkey, D.K., 2010. The velocity-related firing property of hippocampal place cells is dependent on self-movement. Hippocampus 20, 573-583.
75. Machon, R.A., Mednick, S.A., Huttunen, M.O., 1997. Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch. Gen. Psychiatry 54, 322-328.
76. Maister, L., Simons, J., Plaisted-Grant, K., 2013. Executive functions are employed to process episodic and relational memories in children with autism spectrum disorders. Neuropsychology 27, 615-627.
77. Malkova, N., Yu, C., Hsiao, E., Moore, M., Patterson, P., 2012. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav. Immun. 26, 607-616.
78. Markram, H., Lübke, J., Frotscher, M., Sakmann, B., 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science (New York, NY) 275, 213-215.
79. Mathew, I., Gardin, T., Tandon, N., Eack, S., Francis, A., Seidman, L., Clementz, B., Pearlson, G., Sweeney, J., Tamminga, C., Keshavan, M., 2014. Medial temporal lobe structures and hippocampal subfields in psychotic disorders: findings from the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. JAMA Psychiatry 71, 769-777.
80. Maurer, A.P., Vanrhoads, S.R., Sutherland, G.R., Lipa, P., McNaughton, B.L., 2005. Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 15, 841-852.
81. Meyer, U., Feldon, J., 2010. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog. Neurobiol. 90, 285-326.
82. Meyer, U., Feldon, J., Schedlowski, M., Yee, B.K., 2005. Towards an immunoprecipitated neurodevelopmental animal model of schizophrenia. Neurosci. Biobehav. Rev. 29, 913-947.
83. Meyer, U., Knuesel, I., Nyffeler, M., Feldon, J., 2009. Chronic clozapine treatment improves prenatal infection-induced working memory deficits without influencing adult hippocampal neurogenesis. Psychopharmacology 208, 531-543.
84. Meyer, U., Nyffeler, M., Schwendener, S., Knuesel, I., Yee, B.K., Feldon, J., 2008a. Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 33, 441-456.
85. Meyer, U., Nyffeler, M., Yee, B.K., Knuesel, I., Feldon, J., 2008b. Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav. Immun. 22, 469-486.
86. Millan, M.J., Agid, Y., Brune, M., Bullmore, E.T., Carter, C.S., Clayton, N.S., Connor, R., Davis, S., Deakin, B., Derubeis, R.J., Dubois, B., Geyer, M.A., Goodwin, G.M., Gorwood, P., Jay, T.M., Joels, M., Mansuy, I.M., Meyer-Lindenberg, A., Murphy, D., Rolls, E., Saletu, B., Spedding, M., Sweeney, J., Whittington, M., Young, L.J., 2012. Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat. Rev. Drug Discov. 11, 141-168.
87. Morris, R.G., Garrud, P., Rawlins, J.N., O'Keefe, J., 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
88. Muller, R.U., Kubie, J.L., 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951-1968.
89. Muller, R.U., Kubie, J.L., Ranck Jr., J.B., 1987. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950.
90. Mumby, D.G., Gaskin, S., Glenn, M.J., Schramek, T.E., Lehmann, H., 2002. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn. Mem. (Cold Spring Harbor, NY) 9, 49-57.
91. O'Keefe, J., 2007. Hippocampal neurophysiology in the behaving animal. In: Andersen, P., Morris, R., Amaral, D., Bliss, T., O'Keefe, J. (Eds.), The Hippocampus Book. Oxford University Press, NY, pp. 475-548.
92. O'Keefe, J., Burgess, N., 2005. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853-866.
93. O'Keefe, J., Conway, D.H., 1978. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31, 573-590.
94. O'Keefe, J., Dostrovsky, J., 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175.
95. O'Keefe, J., Nadel, L., 1978. The Hippocampus as a Cognitive Map, Oxford University Press.
96. O'Keefe, J., Recce, M.L., 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330.
97. Ozawa, K., Hashimoto, K., Kishimoto, T., Shimizu, E., Ishikura, H., Iyo, M., 2006. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol. Psychiatry 59, 546-554.
98. Parboosing, R., Bao, Y., Shen, L., Schaefer, C.A., Brown, A.S., 2013. Gestational influenza and bipolar disorder in adult offspring. JAMA Psychiatry 70, 677-685.
99. Phillips, K., Bartsch, U., McCarthy, A., Edgar, D., Tricklebank, M., Wafford, K., Jones, M., 2012. Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76, 526-533.
100. Piontkewitz, Y., Arad, M., Weiner, I., 2010. Risperidone administered during asymptomatic period of adolescence prevents the emergence of brain structural pathology and behavioral abnormalities in an animal model of schizophrenia. Schizophr. Bull.
101. Piontkewitz, Y., Assaf, Y., Weiner, I., 2009. Clozapine administration in adolescence prevents postpubertal emergence of brain structural pathology in an animal model of schizophrenia. Biol. Psychiatry 66, 1038-1046.
102. Poucet, B., Thinus-Blanc, C., Muller, R.U., 1994. Place cells in the ventral hippocampus of rats. Neuroreport 5, 2045-2048.
103. Robbe, D., Buzsáki, G., 2009. Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J. Neurosci. 29, 12597-12605.
104. Rosoklija, G., Toomayan, G., Ellis, S.P., Keilp, J., Mann, J.J., Latov, N., Hays, A.P., Dwork, A.J., 2000. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch. Gen. Psychiatry 57, 349-356.
105. Royer, S., Sirota, A., Patel, J., Buzsaki, G., 2010. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 30, 1777-1787.
106. Russell, N.A., Horii, A., Smith, P.F., Darlington, C.L., Bilkey, D.K., 2006. Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J. Neurophysiol. 96, 4-14.
107. Rutishauser, U., Ross, I., Mamelak, A., Schuman, E., 2010. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903-907.
108. Savanthrapadian, S., Wolff, A., Logan, B., Eckert, M., Bilkey, D., Abraham, W., 2013. Enhanced hippocampal neuronal excitability and LTP persistence associated with reduced behavioral flexibility in the maternal immune activation model of schizophrenia. Hippocampus 23, 1395-1409.
109. Savitz, J., Price, J., Drevets, W., 2014. Neuropathological and neuromorphometric abnormalities in bipolar disorder: view from the medial prefrontal cortical network. Neurosci. Biobehav. Rev. 42, 132-147.
110. Servan-Schreiber, D., Cohen, J.D., Steingard, S., 1996. Schizophrenic deficits in the processing of context. A test of a theoretical model. Arch. Gen. Psychiatry 53, 1105-1112.
111. Shapiro, M.L., Tanila, H., Eichenbaum, H., 1997. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624-642.
112. Siegle, J., Wilson, M., 2014. Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus. Elife 3, e03061.
113. Skaggs, W.E., McNaughton, B.L., Wilson, M.A., Barnes, C.A., 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172.
114. Suh, J., Foster, D., Davoudi, H., Wilson, M., Tonegawa, S., 2013. Impaired hippocampal ripple-associated replay in a mouse model of schizophrenia. Neuron 80, 484-493.
115. Thompson, L.T., Best, P.J., 1990. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 509, 299-308.
116. Tian, S.Y., Wang, J.F., Bezchlibnyk, Y.B., Young, L.T., 2007. Immunoreactivity of 43 kDa growth-associated protein is decreased in post mortem hippocampus of bipolar disorder and schizophrenia. Neurosci. Lett. 411, 123-127.
117. Vita, A., De Peri, L., Silenzi, C., Dieci, M., 2006. Brain morphology in first-episode schizophrenia: a meta-analysis of quantitative magnetic resonance imaging studies. Schizophr. Res. 82, 75-88.
118. Webster, M.J., Shannon Weickert, C., Herman, M.M., Hyde, T.M., Kleinman, J.E., 2001. Synaptophysin and GAP-43 mRNA levels in the hippocampus of subjects with schizophrenia. Schizophr. Res. 49, 89-98.
119. Wolff, A.R., Bilkey, D.K., 2008. Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav. Brain Res. 190, 156-159.
120. Wolff, A.R., Bilkey, D.K., 2010. The maternal immune activation (MIA) model of schizophrenia produces pre-pulse inhibition (PPI) deficits in both juvenile and adult rats but these effects are not associated with maternal weight loss. Behav. Brain Res. 213, 323-327.
121. Wolff, A.R., Cheyne, K.R., Bilkey, D.K., 2011. Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia. Behav. Brain Res. 225, 382-387.
122. Wood, S.J., Velakoulis, D., Smith, D.J., Bond, D., Stuart, G.W., McGorry, P.D., Brewer, W.J., Bridle, N., Eritaia, J., Desmond, P., Singh, B., Copolov, D., Pantelis, C., 2001. A longitudinal study of hippocampal volume in first episode psychosis and chronic schizophrenia. Schizophr. Res. 52, 37-46.
123. Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W., David, A.S., Murray, R.M., Bullmore, E.T., 2000. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry 157, 16-25.
124. Zar, J.H., 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.
125. Zuckerman, L., Weiner, I., 2005. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J. Psychiatry. Res. 39, 311-323.