Effects of immune activation during early or late gestation on schizophrenia-related behaviour in adult rat offspring

Brain, Behavior, and Immunity

Volumn 63, Issue , 2017, Pages 8-20

  Meehan, Crystal ^a,b,c,d   Harms, Lauren ^a,b,c,d   Frost, Jade D ^a,b,c,d   Barreto, Rafael ^a   Todd, Juanita ^a,b,c,d   Schall, Ulrich ^b,c,d,e   Shannon Weickert, Cynthia ^c,f,g   Zavitsanou, Katerina ^c   Michie, Patricia T ^a,b,c,d   Hodgson, Deborah M ^a,b,c,d  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Schizophrenia Research Institute   (Australia)

^d HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF NEWCASTLE   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

Author keywords

Dopamine; Gestational timing; Maternal immune activation; Neurodevelopment; Poly (I:C); Rat; Schizophrenia; Sensorimotor gating; Working memory

Indexed keywords

AMPHETAMINE; CORTICOSTERONE; DIZOCILPINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; INTERLEUKIN 6; MESSENGER RNA; NEUROTRANSMITTER RECEPTOR; POLYINOSINIC POLYCYTIDYLIC ACID; TYROSINE 3 MONOOXYGENASE;

ACOUSTIC STARTLE RESPONSE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CAUDATE PUTAMEN; CORPUS STRIATUM; CORTICOSTERONE BLOOD LEVEL; FEMALE; GENE EXPRESSION; IMMUNOREACTIVITY; LOCOMOTION; MALE; MATERNAL IMMUNE ACTIVATION; MEMORY DISORDER; MESENCEPHALON; NONHUMAN; NUCLEUS ACCUMBENS; PREGNANCY; PREPULSE INHIBITION; PRIORITY JOURNAL; PROGENY; PROTEIN BLOOD LEVEL; RAT; SCHIZOPHRENIA; SENSORY GATING; STARTLE REFLEX; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM; WISTAR RAT; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; MATERNAL EXPOSURE; MOTOR ACTIVITY; PHYSIOLOGY; PRENATAL EXPOSURE; SHORT TERM MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FEMALE; MALE; MATERNAL EXPOSURE; MEMORY, SHORT-TERM; MOTOR ACTIVITY; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; REFLEX, STARTLE; SCHIZOPHRENIA;

EID: 85008323025     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.07.144     Document Type: Article

References (93)

1. Andreasen, N.C., Flaum, M., Swayze, V.W. 2nd, Tyrrell, G., Arndt, S., Positive and negative symptoms in schizophrenia. A critical reappraisal. Arch. Gen. Psychiatry 47 (1990), 615–621.
2. Babulas, V., Factor-Litvak, P., Goetz, R., Schaefer, C.A., Brown, A.S., Prenatal exposure to maternal genital and reproductive infections and adult schizophrenia. Am. J. Psychiatry 163 (2006), 927–929.
3. Barch, D.M., Smith, E., The cognitive neuroscience of working memory: relevance to CNTRICS and schizophrenia. Biol. Psychiatry 64 (2008), 11–17.
4. Bayer, S.A., Altman, J., Chapter 2 – Development of the telencephalon: neural stem cells, neurogenesis, and neuronal migration A2. George, Paxinos, (eds.) The Rat Nervous System, 3rd ed., 2004, Academic Press, Burlington, 27–73.
5. Bayer, S.A., Wills, K.V., Triarhou, L.C., Ghetti, B., Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp. Brain Res. 105 (1995), 191–199.
6. Bitanihirwe, B.K., Weber, L., Feldon, J., Meyer, U., Cognitive impairment following prenatal immune challenge in mice correlates with prefrontal cortical AKT1 deficiency. Int. J. Neuropsychopharmacol. 13 (2010), 981–996.
7. Boksa, P., Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24 (2010), 881–897.
8. Bowen, J.M., Chamley, L., Keelan, J.A., Mitchell, M.D., Cytokines of the placenta and extra-placental membranes: roles and regulation during human pregnancy and parturition. Placenta 23 (2002), 257–273.
9. Braff, D.L., Swerdlow, N.R., Geyer, M.A., Symptom correlates of prepulse inhibition deficits in male schizophrenic patients. Am. J. Psychiatry 156 (1999), 596–602.
10. Braff, D.L., Geyer, M.A., Swerdlow, N.R., Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156 (2001), 234–258.
11. Brown, A.S., Derkits, E.J., Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 167 (2010), 261–280.
12. Brown, A.S., Cohen, P., Harkavy-Friedman, J., Babulas, V., Malaspina, D., Gorman, J.M., Susser, E.S., A.E. Bennett Research Award. Prenatal rubella, premorbid abnormalities, and adult schizophrenia. Biol. Psychiatry 49 (2001), 473–486.
13. Brown, A.S., Begg, M.D., Gravenstein, S., Schaefer, C.A., Wyatt, R.J., Bresnahan, M., Babulas, V.P., Susser, E.S., Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 61 (2004), 774–780.
14. Brown, A.S., Hooton, J., Schaefer, C.A., Zhang, H., Petkova, E., Babulas, V., Perrin, M., Gorman, J.M., Susser, E.S., Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. Am. J. Psychiatry 161 (2004), 889–895.
15. Brown, A.S., Schaefer, C.A., Quesenberry, C.P. Jr., Liu, L., Babulas, V.P., Susser, E.S., Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am. J. Psychiatry 162 (2005), 767–773.
16. Buka, S.L., Tsuang, M.T., Torrey, E.F., Klebanoff, M.A., Bernstein, D., Yolken, R.H., Maternal infections and subsequent psychosis among offspring. Arch. Gen. Psychiatry 58 (2001), 1032–1037.
17. Chang, W.C., Hui, C.L., Tang, J.Y., Wong, G.H., Lam, M.M., Chan, S.K., Chen, E.Y., Persistent negative symptoms in first-episode schizophrenia: a prospective three-year follow-up study. Schizophr. Res. 133 (2011), 22–28.
18. Dahlgren, J., Samuelsson, A.M., Jansson, T., Holmang, A., Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation. Pediatr. Res. 60 (2006), 147–151.
19. Dickerson, D.D., Wolff, A.R., Bilkey, D.K., Abnormal long-range neural synchrony in a maternal immune activation animal model of schizophrenia. J. Neurosci. 30 (2010), 12424–12431.
20. Doherty, J.M., Masten, V.L., Powell, S.B., Ralph, R.J., Klamer, D., Low, M.J., Geyer, M.A., Contributions of dopamine D1, D2, and D3 receptor subtypes to the disruptive effects of cocaine on prepulse inhibition in mice. Neuropsychopharmacology 33 (2008), 2648–2656.
21. Dudchenko, P.A., Talpos, J., Young, J., Baxter, M.G., Animal models of working memory: a review of tasks that might be used in screening drug treatments for the memory impairments found in schizophrenia. Neurosci. Biobehav. Rev. 37 (2013), 2111–2124.
22. El-Khodor, B.F., Boksa, P., Birth insult increases amphetamine-induced behavioral responses in the adult rat. Neuroscience 87 (1998), 893–904.
23. Fatemi, S.H., Emamian, E.S., Kist, D., Sidwell, R.W., Nakajima, K., Akhter, P., Shier, A., Sheikh, S., Bailey, K., Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol. Psychiatry 4 (1999), 145–154.
24. Fatemi, S.H., Reutiman, T.J., Folsom, T.D., Huang, H., Oishi, K., Mori, S., Smee, D.F., Pearce, D.A., Winter, C., Sohr, R., Juckel, G., Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr. Res. 99 (2008), 56–70.
25. Fenton, W.S., McGlashan, T.H., Natural history of schizophrenia subtypes. II. Positive and negative symptoms and long-term course. Arch. Gen. Psychiatry 48 (1991), 978–986.
26. Flores, G., Wood, G.K., Liang, J.-J., Quirion, R., Srivastava, L.K., Enhanced Amphetamine sensitivity and increased expression of dopamine D2 receptors in postpubertal rats after neonatal excitotoxic lesions of the medial prefrontal cortex. J. Neurosci. 16 (1996), 7366–7375.
27. Foldi, C.J., Eyles, D.W., McGrath, J.J., Burne, T.H., Advanced paternal age is associated with alterations in discrete behavioural domains and cortical neuroanatomy of C57BL/6J mice. Eur. J. Neurosci. 31 (2010), 556–564.
28. Fortier, M.E., Joober, R., Luheshi, G.N., Boksa, P., Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J. Psychiatr. Res. 38 (2004), 335–345.
29. Gates, M.A., Torres, E.M., White, A., Fricker-Gates, R.A., Dunnett, S.B., Re-examining the ontogeny of substantia nigra dopamine neurons. Eur. J. Neurosci. 23 (2006), 1384–1390.
30. Geyer, M.A., Krebs-Thomson, K., Braff, D.L., Swerdlow, N.R., Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 156 (2001), 117–154.
31. Gogos, A., van den Buuse, M., Comparing the effects of 17β-oestradiol and the selective oestrogen receptor modulators, raloxifene and tamoxifen, on prepulse inhibition in female rats. Schizophr. Res., 2015.
32. Gogos, A., Kwek, P., Chavez, C., van den Buuse, M., Estrogen treatment blocks 8-hydroxy-2-dipropylaminotetralin- and apomorphine-induced disruptions of prepulse inhibition: involvement of dopamine D1 or D2 or serotonin 5-HT1A, 5-HT2A, or 5-HT7 receptors. J. Pharmacol. Exp. Ther. 333 (2010), 218–227.
33. Harms, L., Mismatch responses and deviance detection in N-methyl-D-aspartate (NMDA) receptor hypofunction and developmental models of schizophrenia. Biol. Psychol., 2015.
34. Harms, L.R., Eyles, D.W., McGrath, J.J., Mackay-Sim, A., Burne, T.H., Developmental vitamin D deficiency alters adult behaviour in 129/SvJ and C57BL/6J mice. Behav. Brain Res. 187 (2008), 343–350.
35. Harms, L., Fulham, W.R., Todd, J., Budd, T.W., Hunter, M., Meehan, C., Penttonen, M., Schall, U., Zavitsanou, K., Hodgson, D.M., Michie, P.T., Mismatch negativity (MMN) in freely-moving rats with several experimental controls. PLoS One, 9, 2014, e110892.
36. Howes, O.D., Kapur, S., The dopamine hypothesis of schizophrenia: version III–the final common pathway. Schizophr. Bull. 35 (2009), 549–562.
37. Howland, J.G., Cazakoff, B.N., Zhang, Y., Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 201 (2012), 184–198.
38. Karl, T., Burne, T.H., Van den Buuse, M., Chesworth, R., Do transmembrane domain neuregulin 1 mutant mice exhibit a reliable sensorimotor gating deficit?. Behav. Brain Res. 223 (2011), 336–341.
39. Kay, S.R., Opler, L.A., Fiszbein, A., Significance of positive and negative syndromes in chronic schizophrenia. Br. J. Psychiatry 149 (1986), 439–448.
40. Kesby, J.P., Cui, X., O'Loan, J., McGrath, J.J., Burne, T.H., Eyles, D.W., Developmental vitamin D deficiency alters dopamine-mediated behaviors and dopamine transporter function in adult female rats. Psychopharmacology 208 (2010), 159–168.
41. Kesby, J.P., O'Loan, J.C., Alexander, S., Deng, C., Huang, X.F., McGrath, J.J., Eyles, D.W., Burne, T.H., Developmental vitamin D deficiency alters MK-801-induced behaviours in adult offspring. Psychopharmacology 220 (2012), 455–463.
42. Kulkarni, J., Gavrilidis, E., Worsley, R., Hayes, E., Role of estrogen treatment in the management of schizophrenia. CNS Drugs 26 (2012), 549–557.
43. Lante, F., Meunier, J., Guiramand, J., Maurice, T., Cavalier, M., de Jesus Ferreira, M.C., Aimar, R., Cohen-Solal, C., Vignes, M., Barbanel, G., Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain. Free Radical Biol. Med. 42 (2007), 1231–1245.
44. Lante, F., Meunier, J., Guiramand, J., De Jesus Ferreira, M.C., Cambonie, G., Aimar, R., Cohen-Solal, C., Maurice, T., Vignes, M., Barbanel, G., Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus 18 (2008), 602–609.
45. Lee, J., Park, S., Working memory impairments in schizophrenia: a meta-analysis. J. Abnorm. Psychol. 114 (2005), 599–611.
46. Lewis, D.A., Lieberman, J.A., Catching up on schizophrenia: natural history and neurobiology. Neuron 28 (2000), 325–334.
47. Lewis, D.A., Moghaddam, B., Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch. Neurol. 63 (2006), 1372–1376.
48. Li, Q., Cheung, C., Wei, R., Hui, E.S., Feldon, J., Meyer, U., Chung, S., Chua, S.E., Sham, P.C., Wu, E.X., McAlonan, G.M., Prenatal immune challenge is an environmental risk factor for brain and behavior change relevant to schizophrenia: evidence from MRI in a mouse model. PLoS One, 4, 2009, e6354.
49. Lieberman, J.A., Kane, J.M., Alvir, J., Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology 91 (1987), 415–433.
50. Light, G.A., Swerdlow, N.R., Future clinical uses of neurophysiological biomarkers to predict and monitor treatment response for schizophrenia. Ann. N. Y. Acad. Sci. 1344 (2015), 105–119.
51. Lyon, L., Saksida, L.M., Bussey, T.J., 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.
52. McGrath, J., Saha, S., Welham, J., El Saadi, O., MacCauley, C., Chant, D., A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med., 2, 2004, 13.
53. Mendrek, A., Mancini-Marie, A., Sex/gender differences in the brain and cognition in schizophrenia. Neurosci. Biobehav. Rev., 2015.
54. Meyer, U., Prenatal poly(i:C) exposure and other developmental immune activation models in rodent systems. Biol. Psychiatry 75 (2014), 307–315.
55. Meyer, U., Feldon, J., To poly(I:C) or not to poly(I:C): advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology 62 (2012), 1308–1321.
56. Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B.K., Feldon, J., The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 26 (2006), 4752–4762.
57. Meyer, U., Murray, P.J., Urwyler, A., Yee, B.K., Schedlowski, M., Feldon, J., Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol. Psychiatry 13 (2008), 208–221.
58. Meyer, U., Nyffeler, M., Schwendener, S., Knuesel, I., Yee, B.K., Feldon, J., Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 33 (2008), 441–456.
59. Meyer, U., Nyffeler, M., Yee, B.K., Knuesel, I., Feldon, J., Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav. Immun. 22 (2008), 469–486.
60. Missault, S., Van den Eynde, K., Vanden Berghe, W., Fransen, E., Weeren, A., Timmermans, J.P., Kumar-Singh, S., Dedeurwaerdere, S., The risk for behavioural deficits is determined by the maternal immune response to prenatal immune challenge in a neurodevelopmental model. Brain Behav. Immun. 42 (2014), 138–146.
61. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B., Seeburg, P.H., Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12 (1994), 529–540.
62. Morgan, V.A., Castle, D.J., Jablensky, A.V., Do women express and experience psychosis differently from men? Epidemiological evidence from the Australian National Study of Low Prevalence (Psychotic) Disorders. Aust. N. Z. J. Psychiatry 42 (2008), 74–82.
63. O'Leary, C., Desbonnet, L., Clarke, N., Petit, E., Tighe, O., Lai, D., Harvey, R., Waddington, J.L., O'Tuathaigh, C., Phenotypic effects of maternal immune activation and early postnatal milieu in mice mutant for the schizophrenia risk gene neuregulin-1. Neuroscience 277 (2014), 294–305.
64. Owen, M.J., Craddock, N., O'Donovan, M.C., Schizophrenia: genes at last?. Trends Genet. 21 (2005), 518–525.
65. Ozawa, K., Hashimoto, K., Kishimoto, T., Shimizu, E., Ishikura, H., Iyo, M., 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 (2006), 546–554.
66. Paxinos, G., Watson, C., The Rat Brain in Stereotaxic Coordinates. 2005, Elsevier Academic Press.
67. Piontkewitz, Y., Arad, M., Weiner, I., Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat. Biol. Psychiatry 70 (2011), 842–851.
68. Richetto, J., Calabrese, F., Meyer, U., Riva, M.A., Prenatal versus postnatal maternal factors in the development of infection-induced working memory impairments in mice. Brain Behav. Immun. 33 (2013), 190–200.
69. Ring, N., Tantam, D., Montague, L., Newby, D., Black, D., Morris, J., Gender differences in the incidence of definite schizophrenia and atypical psychosis–focus on negative symptoms of schizophrenia. Acta Psychiatr. Scand. 84 (1991), 489–496.
70. Romero, E., Guaza, C., Castellano, B., Borrell, J., Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol. Psychiatry 15 (2010), 372–383.
71. Samuelsson, A.M., Jennische, E., Hansson, H.A., Holmang, A., Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 (2006), R1345–R1356.
72. Savanthrapadian, S., Wolff, A.R., Logan, B.J., Eckert, M.J., Bilkey, D.K., Abraham, W.C., Enhanced hippocampal neuronal excitability and LTP persistence associated with reduced behavioral flexibility in the maternal immune activation model of schizophrenia. Hippocampus 23 (2013), 1395–1409.
73. Schultz, S.K., Miller, D.D., Oliver, S.E., Arndt, S., Flaum, M., Andreasen, N.C., The life course of schizophrenia: age and symptom dimensions. Schizophr. Res. 23 (1997), 15–23.
74. Shi, L., Fatemi, S.H., Sidwell, R.W., Patterson, P.H., Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23 (2003), 297–302.
75. Sorensen, H.J., Mortensen, E.L., Reinisch, J.M., Mednick, S.A., Association between prenatal exposure to bacterial infection and risk of schizophrenia. Schizophr. Bull. 35 (2009), 631–637.
76. Suvisaari, J., Haukka, J., Tanskanen, A., Hovi, T., Lonnqvist, J., Association between prenatal exposure to poliovirus infection and adult schizophrenia. Am. J. Psychiatry 156 (1999), 1100–1102.
77. Torrey, E.F., Rawlings, R., Waldman, I.N., Schizophrenic births and viral diseases in two states. Schizophr. Res. 1 (1988), 73–77.
78. Vorhees, C.V., Graham, D.L., Braun, A.A., Schaefer, T.L., Skelton, M.R., Richtand, N.M., Williams, M.T., Prenatal immune challenge in rats: altered responses to dopaminergic and glutamatergic agents, prepulse inhibition of acoustic startle, and reduced route-based learning as a function of maternal body weight gain after prenatal exposure to poly IC. Synapse 66 (2012), 725–737.
79. Vorhees, C.V., Graham, D.L., Braun, A.A., Schaefer, T.L., Skelton, M.R., Richtand, N.M., Williams, M.T., Prenatal immune challenge in rats: effects of polyinosinic-polycytidylic acid on spatial learning, prepulse inhibition, conditioned fear, and responses to MK-801 and amphetamine. Neurotoxicol. Teratol. 47 (2015), 54–65.
80. Vuillermot, S., Weber, L., Feldon, J., Meyer, U., A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J. Neurosci. 30 (2010), 1270–1287.
81. Weickert, T.W., Weinberg, D., Lenroot, R., Catts, S.V., Wells, R., Vercammen, A., O'Donnell, M., Galletly, C., Liu, D., Balzan, R., Short, B., Pellen, D., Curtis, J., Carr, V.J., Kulkarni, J., Schofield, P.R., Weickert, C.S., Adjunctive raloxifene treatment improves attention and memory in men and women with schizophrenia. Mol. Psychiatry 20 (2015), 685–694.
82. Wilson, C., Terry, A.V. Jr., Neurodevelopmental animal models of schizophrenia: role in novel drug discovery and development. Clin. Schizophr. Relat. Psychoses 4 (2010), 124–137.
83. Wolff, A.R., Bilkey, D.K., Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav. Brain Res. 190 (2008), 156–159.
84. Wolff, A.R., Bilkey, D.K., 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 (2010), 323–327.
85. Wolff, A.R., Cheyne, K.R., Bilkey, D.K., Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia. Behav. Brain Res. 225 (2011), 382–387.
86. Workman, A.D., Charvet, C.J., Clancy, B., Darlington, R.B., Finlay, B.L., Modeling transformations of neurodevelopmental sequences across mammalian species. J. Neurosci. 33 (2013), 7368–7383.
87. Xie, F., Xiao, P., Chen, D., Xu, L., Zhang, B., MiRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol. Biol, 2012.
88. Yee, N., Schwarting, R.K., Fuchs, E., Wohr, M., Increased affective ultrasonic communication during fear learning in adult male rats exposed to maternal immune activation. J. Psychiatr. Res. 46 (2012), 1199–1205.
89. Zhang, Y., Cazakoff, B.N., Thai, C.A., Howland, J.G., Prenatal exposure to a viral mimetic alters behavioural flexibility in male, but not female, rats. Neuropharmacology 62 (2012), 1299–1307.
90. Zourbas, S., Dubanchet, S., Martal, J., Chaouat, G., Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin. Exp. Immunol. 126 (2001), 519–528.
91. Zuckerman, L., Weiner, I., Post-pubertal emergence of disrupted latent inhibition following prenatal immune activation. Psychopharmacology 169 (2003), 308–313.
92. Zuckerman, L., Weiner, I., Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J. Psychiatr. Res. 39 (2005), 311–323.
93. Zuckerman, L., Rehavi, M., Nachman, R., Weiner, I., Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 28 (2003), 1778–1789.