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Neurochemical Research

, Volume 44, Issue 3, pp 609–616 | Cite as

Disturbance of Metabotropic Glutamate Receptor-Mediated Long-Term Depression (mGlu-LTD) of Excitatory Synaptic Transmission in the Rat Hippocampus After Prenatal Immune Challenge

  • Mélanie Cavalier
  • Azza Ben Sedrine
  • Lea Thevenet
  • Nadine Crouzin
  • Janique Guiramand
  • Marie-Céleste de Jésus Ferreira
  • Catherine Cohen-Solal
  • Gérard Barbanel
  • Michel VignesEmail author
Original Paper

Abstract

Maternal immune challenge has proved to induce moderate to severe behavioral disabilities in the offspring. Cognitive/behavioral deficits are supported by changes in synaptic plasticity in different brain areas. We have reported previously that prenatal exposure to bacterial LPS could induce inhibition of hippocampal long-term potentiation (LTP) in the CA1 area of the juvenile/adult male offspring associated with spatial learning inabilities. Nevertheless, deficits in plasticity could be observed at earlier stages as shown by the early loss of long-term depression (LTD) in immature animals. Moreover, aberrant forms of plasticity were also evidenced such as the transient occurrence of LTP instead of LTD in 15–25 day-old animals. This switch from LTD to LTP seemed to involve the activation of metabotropic glutamate receptor subtype 1 and 5 (mGlu1/5). We have thus investigated here whether the long-term depression elicited by the direct activation of these receptors (mGlu-LTD) with a selective agonist was also disturbed after prenatal stress. We find that in prenatally stressed rats, mGlu1/5 stimulation elicits long-term potentiation (mGlu-LTP) independently of N-methyl-d-aspartate receptors. Both mGlu5 and mGlu1 receptors are involved in this switch of plasticity. Moreover, this mGlu-LTP is still observed at later developmental stages than previously reported, i.e. after 25 day-old. In addition, increasing synaptic GABA with tiagabine tends to inhibit mGlu-LTP occurrence. By contrast, long-term depression induced with the activation of CB1 cannabinoid receptor is unaffected by prenatal stress. Therefore, prenatal stress drastically alters mGlu1/5-associated plasticity throughout development. MGlu-mediated plasticity is an interesting parameter to probe the long-lasting deficits reported in this model.

Keywords

Prenatal stress Hippocampus mGlu1/5 LTD LTP Synaptic plasticity Dihydroxyphenylglycine 

References

  1. 1.
    Atladóttir HO, Thorsen P, Østergaard L, Schendel DE, Lemcke S, Abdallah M, Parner ET (2010) Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 40:1423–1430CrossRefPubMedGoogle Scholar
  2. 2.
    Brown AS, Derkits EJ (2010) Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 167:261–280CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hagberg H, Gressens P, Mallard C (2012) Inflammation during fetal and neonatal life: implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol 71:444–457CrossRefPubMedGoogle Scholar
  4. 4.
    Boksa P (2010) Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 24:881–897CrossRefPubMedGoogle Scholar
  5. 5.
    Lanté F, Meunier J, Guiramand J, Maurice T, Cavalier M, de Jesus Ferreira MC, Aimar R, Cohen-Solal C, Vignes M, Barbanel G (2007) Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain. Free Radic Biol Med 42:1231–1245CrossRefPubMedGoogle Scholar
  6. 6.
    Lanté F, Meunier J, Guiramand J, De Jesus Ferreira MC, Cambonie G, Aimar R, Cohen-Solal C, Maurice T, Vignes M, Barbanel G (2008) Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus 18:602–609CrossRefPubMedGoogle Scholar
  7. 7.
    Escobar M, Crouzin N, Cavalier M, Quentin J, Roussel J, Lanté F, Batista-Novais AR, Cohen-Solal C, De Jesus Ferreira MC, Guiramand J, Barbanel G, Vignes M (2011) Early, time-dependent disturbances of hippocampal synaptic transmission and plasticity after in utero immune challenge. Biol Psychiatry 70:992–999CrossRefPubMedGoogle Scholar
  8. 8.
    Rideau Batista Novais A, Crouzin N, Cavalier M, Boubal M, Guiramand J, Cohen-Solal C, de Jesus Ferreira MC, Cambonie G, Vignes M, Barbanel G (2014) Tiagabine improves hippocampal long-term depression in rat pups subjected to prenatal inflammation. PLoS ONE 9(9):e106302.  https://doi.org/10.1371/journal.pone.0106302 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Volianskis A, France G, Jensen MS, Bortolotto ZA, Jane DE, Collingridge GL (2015) Long-term potentiation and the role of N-methyl-D-aspartate receptors. Brain Res 1621:5–16CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254–1257CrossRefPubMedGoogle Scholar
  11. 11.
    Fitzjohn SM, Kingston AE, Lodge D, Collingridge GL (1999) DHPG-induced LTD in area CA1 of juvenile rat hippocampus; characterisation and sensitivity to novel mGlu receptor antagonists. Neuropharmacology 38:1577–1583CrossRefPubMedGoogle Scholar
  12. 12.
    Lüscher C, Huber KM (2010) Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65:445–459CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473CrossRefPubMedGoogle Scholar
  14. 14.
    Bear MF, Huber KM, Warren ST (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci 27:370–377CrossRefPubMedGoogle Scholar
  15. 15.
    Knackstedt LA, Trantham-Davidson HL, Schwendt M (2014) The role of ventral and dorsal striatum mGluR5 in relapse to cocaine-seeking and extinction learning. Addict Biol 19:87–101CrossRefPubMedGoogle Scholar
  16. 16.
    Hoffmann HM, Crouzin N, Moreno E, Raivio N, Fuentes S, McCormick PJ, Ortiz J, Vignes M (2016) Long-lasting impairment of mGluR5-activated intracellular pathways in the striatum after withdrawal of cocaine self-administration. Int J Neuropsychopharmacol.  https://doi.org/10.1093/ijnp/pyw086 PubMedPubMedCentralGoogle Scholar
  17. 17.
    D’Antoni S, Spatuzza M, Bonaccorso CM, Musumeci SA, Ciranna L, Nicoletti F, Huber KM, Catania MV (2014) Dysregulation of group-I metabotropic glutamate (mGlu) receptor mediated signalling in disorders associated with Intellectual Disability and Autism. Neurosci Biobehav Rev 46:228–241CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Heuschkel MO, Fejtl M, Raggenbass M, Bertrand D, Renaud P (2002) A three-dimensional multi-electrode array for multi-site stimulation and recording in acute brain slices. J Neurosci Methods 114:135–148CrossRefPubMedGoogle Scholar
  19. 19.
    Lanté F, de Jésus Ferreira MC, Guiramand J, Récasens M, Vignes M (2006) Low-frequency stimulation induces a new form of LTP, metabotropic glutamate (mGlu5) receptor- and PKA-dependent, in the CA1 area of the rat hippocampus. Hippocampus 16:345–360CrossRefPubMedGoogle Scholar
  20. 20.
    Kopanitsa MV1, Afinowi NO, Grant SG (2006) Recording long-term potentiation of synaptic transmission by three-dimensional multi-electrode arrays. BMC Neurosci 7:61CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Kingston AE, O’Neill MJ, Bond A, Bruno V, Battaglia G, Nicoletti F, Harris JR, Clark BP, Monn JA, Lodge D, Schoepp DD (1999) Neuroprotective actions of novel and potent ligands of group I and group II metabotropic glutamate receptors. Ann N Y Acad Sci 890:438–449CrossRefPubMedGoogle Scholar
  22. 22.
    Gasparini F, Lingenhöhl K, Stoehr N, Flor PJ, Heinrich M, Vranesic I, Biollaz M, Allgeier H, Heckendorn R, Urwyler S, Varney MA, Johnson EC, Hess SD, Rao SP, Sacaan AI, Santori EM, Veliçelebi G, Kuhn R (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology 38:1493–1503CrossRefPubMedGoogle Scholar
  23. 23.
    Izumi Y, Zorumski CF (2012) NMDA receptors, mGluR5, and endocannabinoids are involved in a cascade leading to hippocampal long-term depression. Neuropsychopharmacology 37:609–617CrossRefPubMedGoogle Scholar
  24. 24.
    Perroy J, Raynaud F, Homburger V, Rousset MC, Telley L, Bockaert J, Fagni L (2008) Direct interaction enables cross-talk between ionotropic and group I metabotropic glutamate receptors. J Biol Chem 283:6799–6805CrossRefPubMedGoogle Scholar
  25. 25.
    Guilmatre A, Huguet G, Delorme R, Bourgeron T (2014) The emerging role of SHANK genes in neuropsychiatric disorders. Dev Neurobiol 74:113–122CrossRefPubMedGoogle Scholar
  26. 26.
    Iasevoli F, Tomasetti C, Buonaguro EF, de Bartolomeis A (2014) The glutamatergic aspects of schizophrenia molecular pathophysiology: role of the postsynaptic density, and implications for treatment. Curr Neuropharmacol 12:219–238CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Goh JJ, Manahan-Vaughan D (2013) Endogenous hippocampal LTD that is enabled by spatial object recognition requires activation of NMDA receptors and the metabotropic glutamate receptor, mGlu5. Hippocampus 23:129–138CrossRefPubMedGoogle Scholar
  28. 28.
    Rook JM, Xiang Z, Lv X, Ghoshal A, Dickerson JW, Bridges TM, Johnson KA, Foster DJ, Gregory KJ, Vinson PN, Thompson AD, Byun N, Collier RL, Bubser M, Nedelcovych MT, Gould RW, Stauffer SR, Daniels JS, Niswender CM, Lavreysen H, Mackie C, Conde-Ceide S, Alcazar J, Bartolomé-Nebreda JM, Macdonald GJ, Talpos JC, Steckler T, Jones CK, Lindsley CW, Conn PJ (2015) Biased mGlu5-positive allosteric modulators provide in vivo efficacy without potentiating mGlu5 modulation of NMDAR currents. Neuron 86:1029–1040CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Vicidomini C, Ponzoni L, Lim D, Schmeisser MJ, Reim D, Morello N, Orellana D, Tozzi A, Durante V, Scalmani P, Mantegazza M, Genazzani AA, Giustetto M, Sala M, Calabresi P, Boeckers TM, Sala C, Verpelli C (2017) Pharmacological enhancement of mGlu5 receptors rescues behavioral deficits in SHANK3 knock-out mice. Mol Psychiatry 22:689–702CrossRefPubMedGoogle Scholar
  30. 30.
    Degos V, Peineau S, Nijboer C, Kaindl AM, Sigaut S, Favrais G, Plaisant F, Teissier N, Gouadon E, Lombet A, Saliba E, Collingridge GL, Maze M, Nicoletti F, Heijnen C, Mantz J, Kavelaars A, Gressens P (2013) G protein-coupled receptor kinase 2 and group I metabotropic glutamate receptors mediate inflammation-induced sensitization to excitotoxic neurodegeneration. Ann Neurol 73:667–678CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Mélanie Cavalier
    • 1
  • Azza Ben Sedrine
    • 1
  • Lea Thevenet
    • 1
  • Nadine Crouzin
    • 1
  • Janique Guiramand
    • 1
  • Marie-Céleste de Jésus Ferreira
    • 1
  • Catherine Cohen-Solal
    • 1
  • Gérard Barbanel
    • 1
  • Michel Vignes
    • 1
    Email author
  1. 1.UMR5247 Institut des Biomolécules Max Mousseron – University of Montpellier-CNRS-ENSCM, Team ‘Pharmacochemistry of Synaptic transmission and Neuroprotection’University of Montpellier-Sciences FacultyMontpellier Cedex 05France

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