Early Alterations in Hippocampal Circuitry and Theta Rhythm Generation in a Mouse Model of Prenatal Infection: Implications for Schizophrenia

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2012 Jan 13

PMID 22238649

Citations 25

Authors

Guillaume Ducharme

Germaine C Lowe

Romain Goutagny

Sylvain Williams

Affiliations

Soon will be listed here.

Abstract

Post-mortem studies suggest that GABAergic neurotransmission is impaired in schizophrenia. However, it remains unclear if these changes occur early during development and how they impact overall network activity. To investigate this, we used a mouse model of prenatal infection with the viral mimic, polyriboinosinic-polyribocytidilic acid (poly I:C), a model based on epidemiological evidence that an immune challenge during pregnancy increases the prevalence of schizophrenia in the offspring. We found that prenatal infection reduced the density of parvalbumin- but not somatostatin-positive interneurons in the CA1 area of the hippocampus and strongly reduced the strength of inhibition early during postnatal development. Furthermore, using an intact hippocampal preparation in vitro, we found reduced theta oscillation generated in the CA1 area. Taken together, these results suggest that redistribution in excitatory and inhibitory transmission locally in the CA1 is associated with a significant alteration in network function. Furthermore, given the role of theta rhythm in memory, our results demonstrate how a risk factor for schizophrenia can affect network function early in development that could contribute to cognitive deficits observed later in the disease.

Citing Articles

GABAergic and inflammatory changes in the frontal cortex following neonatal PCP plus isolation rearing, as a dual-hit neurodevelopmental model for schizophrenia.

Cale J, Chauhan E, Cleaver J, Fusciardi A, McCann S, Waters H Mol Neurobiol. 2024; 61(9):6968-6983.

PMID: 38363536 PMC: 11339149. DOI: 10.1007/s12035-024-03987-y.

Maternal immune activation and role of placenta in the prenatal programming of neurodevelopmental disorders.

Woods R, Lorusso J, Fletcher J, ElTaher H, McEwan F, Harris I Neuronal Signal. 2023; 7(2):NS20220064.

PMID: 37332846 PMC: 10273029. DOI: 10.1042/NS20220064.

Development of network oscillations through adolescence in male and female rats.

Sibilska S, Mofleh R, Kocsis B Front Cell Neurosci. 2023; 17:1135154.

PMID: 37213214 PMC: 10196069. DOI: 10.3389/fncel.2023.1135154.

Maternal immune activation-induced proBDNF-mediated neural information processing dysfunction at hippocampal CA3-CA1 synapses associated with memory deficits in offspring.

Sun W, Mei Y, Li X, Yang Y, An L Front Cell Dev Biol. 2022; 10:1018586.

PMID: 36438556 PMC: 9691851. DOI: 10.3389/fcell.2022.1018586.

Disorganization of Oscillatory Activity in Animal Models of Schizophrenia.

Speers L, Bilkey D Front Neural Circuits. 2021; 15:741767.

PMID: 34675780 PMC: 8523827. DOI: 10.3389/fncir.2021.741767.

References

Lodge D, Behrens M, Grace A . A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci. 2009; 29(8):2344-54. PMC: 2754752. DOI: 10.1523/JNEUROSCI.5419-08.2009. View

Meyer U, Feldon J, Schedlowski M, Yee B . Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev. 2005; 29(6):913-47. DOI: 10.1016/j.neubiorev.2004.10.012. View

Xiao J, Buka S, Cannon T, Suzuki Y, Viscidi R, Torrey E . Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes Infect. 2009; 11(13):1011-8. DOI: 10.1016/j.micinf.2009.07.007. View

Francois J, Ferrandon A, Koning E, Angst M, Sandner G, Nehlig A . Selective reorganization of GABAergic transmission in neonatal ventral hippocampal-lesioned rats. Int J Neuropsychopharmacol. 2009; 12(8):1097-110. DOI: 10.1017/S1461145709009985. View

Gonzalez Campo C, Sinagra M, Verrier D, Manzoni O, Chavis P . Reelin secreted by GABAergic neurons regulates glutamate receptor homeostasis. PLoS One. 2009; 4(5):e5505. PMC: 2675077. DOI: 10.1371/journal.pone.0005505. View

Boutros N, Arfken C, Galderisi S, Warrick J, Pratt G, Iacono W . The status of spectral EEG abnormality as a diagnostic test for schizophrenia. Schizophr Res. 2007; 99(1-3):225-37. PMC: 2288752. DOI: 10.1016/j.schres.2007.11.020. View

Margarita Behrens M, Ali S, Dao D, Lucero J, Shekhtman G, Quick K . Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science. 2007; 318(5856):1645-7. DOI: 10.1126/science.1148045. View

Gonzalez-Burgos G, Hashimoto T, Lewis D . Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep. 2010; 12(4):335-44. PMC: 2919752. DOI: 10.1007/s11920-010-0124-8. View

Atallah B, Scanziani M . Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron. 2009; 62(4):566-77. PMC: 2702525. DOI: 10.1016/j.neuron.2009.04.027. View

10.

Goutagny R, Jackson J, Williams S . Self-generated theta oscillations in the hippocampus. Nat Neurosci. 2009; 12(12):1491-3. DOI: 10.1038/nn.2440. View

11.

Nullmeier S, Panther P, Dobrowolny H, Frotscher M, Zhao S, Schwegler H . Region-specific alteration of GABAergic markers in the brain of heterozygous reeler mice. Eur J Neurosci. 2011; 33(4):689-98. DOI: 10.1111/j.1460-9568.2010.07563.x. View

12.

Buka S, Cannon T, Torrey E, Yolken R . Maternal exposure to herpes simplex virus and risk of psychosis among adult offspring. Biol Psychiatry. 2007; 63(8):809-15. DOI: 10.1016/j.biopsych.2007.09.022. View

13.

Meyer U, Nyffeler M, Yee B, 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. 2007; 22(4):469-86. DOI: 10.1016/j.bbi.2007.09.012. View

14.

Haider B, Duque A, Hasenstaub A, McCormick D . Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci. 2006; 26(17):4535-45. PMC: 6674060. DOI: 10.1523/JNEUROSCI.5297-05.2006. View

15.

Bitanihirwe B, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U . Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology. 2010; 35(12):2462-78. PMC: 3055332. DOI: 10.1038/npp.2010.129. View

16.

Reynolds G, Beasley C . GABAergic neuronal subtypes in the human frontal cortex--development and deficits in schizophrenia. J Chem Neuroanat. 2001; 22(1-2):95-100. DOI: 10.1016/s0891-0618(01)00113-2. View

17.

Benes F, Khan Y, VINCENT S, Wickramasinghe R . Differences in the subregional and cellular distribution of GABAA receptor binding in the hippocampal formation of schizophrenic brain. Synapse. 1996; 22(4):338-49. DOI: 10.1002/(SICI)1098-2396(199604)22:4<338::AID-SYN5>3.0.CO;2-C. View

18.

Karlsgodt K, Robleto K, Trantham-Davidson H, Jairl C, Cannon T, Lavin A . Reduced dysbindin expression mediates N-methyl-D-aspartate receptor hypofunction and impaired working memory performance. Biol Psychiatry. 2010; 69(1):28-34. PMC: 4204919. DOI: 10.1016/j.biopsych.2010.09.012. View

19.

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. 2003; 28(10):1778-89. DOI: 10.1038/sj.npp.1300248. View

20.

Hashimoto T, Volk D, Eggan S, Mirnics K, Pierri J, Sun Z . Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci. 2003; 23(15):6315-26. PMC: 6740534. View