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Journal of Cellular and Molecular Medicine logoLink to Journal of Cellular and Molecular Medicine
. 2007 May 1;8(1):31–37. doi: 10.1111/j.1582-4934.2004.tb00257.x

Plasticity of GABAergic synapses in the neonatal rat hippocampus

J‐L Gaïarsa 1,
PMCID: PMC6740258  PMID: 15090258

Abstract

While the development and plasticity of excitatory synaptic connections have been studied into detail, little is known about the development of inhibitory synapses. As proposed for excitatory synapses, recent studies have indicated that activity‐dependent forms of synaptic plasticity, such as long‐term potentiation and long‐term depression, may play a role in the establishment of functional inhibitory synaptic connections. Here, I review these different forms of plasticity and focus on their possible role in the developing neuronal network.

Keywords: synaptic plasticity, GABA, glycine, calcium

References

  • 1. Shatz C.J., Impulse activity and the patterning of connections during CNS development, Neuron, 5: 745–756, 1990. [DOI] [PubMed] [Google Scholar]
  • 2. Constantine‐Paton M., Cline H.T., LTP and activity dependent synaptogenesis: the more alike they are, the more different they become, Curr.Opin.Neurobiol., 8: 139–148, 1998. [DOI] [PubMed] [Google Scholar]
  • 3. Lo Y.J., Poo M.M., Activity‐dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science, 254: 1019–1021, 1991. [DOI] [PubMed] [Google Scholar]
  • 4. Lo Y.J., Poo M.M., Heterosynaptic suppression of the developing neuromuscular synapses in culture. J.Neurosci., 14: 4684–4693, 1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Kirkwood A., Lee H.K., Bear M.F., Co‐regulation of long‐term potentiation and experience‐dependet synaptic plasticity in visual cortex by age and experience, Nature, 375: 328–331, 1995. [DOI] [PubMed] [Google Scholar]
  • 6. Sanes D.H., Siverls V., The development and specificity of inhibitory axonal arborizations in the lateral superior olive, J. Neurobiol., 22: 837–854, 1991. [DOI] [PubMed] [Google Scholar]
  • 7. Sanes D.H., Tackacs C. Actvity‐dependent refinement of inhibitory connections. Eur. J. Neurosci., 5: 570–574, 1993. [DOI] [PubMed] [Google Scholar]
  • 8. Marty S., Wehrlé R., Sotelo C., Neuronal activity and brain‐derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci., 20: 8087–8095, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Seil F.J., Drake‐Baumann R., Reduced cortical inhibitory synaptogenesis in organotypic cerebellar cultures developing in the absence of neuronal activity. J Comp.Neurol., 342: 366–377, 1994. [DOI] [PubMed] [Google Scholar]
  • 10. Micheva K.D., Beaulieu C., An anatomical substrate for experience‐dependent plasticity of the rat barrel field cortex, Proc.Natl.Acad.Sci.U.S.A., 92: 11834–11838, 1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Hendry S.H., Jones E.G., Activity‐dependent regulation of GABA expression in the visual cortex of adult monkey, Neuron, 1: 701–712, 1988. [DOI] [PubMed] [Google Scholar]
  • 12. Benevento L.A., Bakkum B.W., Cohen R.S., Gammaaminobutyric acid and somatostatin immunorecativity in the visual cortex of normal and dark‐reared rats, Brain Res., 689: 172–182, 1995. [DOI] [PubMed] [Google Scholar]
  • 13. Morales B., Choi S.Y., Kirkwood A., Dark rearing alters the development of GABAergic transmission in visual cortex, J.Neurosci., 22: 8084–8090, 2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14. Rutherford L.C., DeWan A., Lauer H.M., Turrigiano G.G., Brain‐derived neurotrophic factor mediates the activity‐dependent regulation of inhibition in neocortical cultures. J.Neurosci., 17: 4527–4535, 1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15. Galante M., Nistri A., Ballerini L., Opposite changes in synaptic activity of organotypic rat spinal cord cultures after chronic block of AMPA/kainate or glycine and GABAA receptors, J.Physiol, 523: 639–651, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16. Aamodt M.A., Shi J., Colonnese M.T., Veras W., Constantine‐Paton M., Chronic NMDA exprosure accelerated development of GABAergic inhibition in the suprior colliculus. J.Neurophysiol., 83: 1580–1591, 2000. [DOI] [PubMed] [Google Scholar]
  • 17. Kotak V.C., Sanes D.H., Long‐lasting inhibitory synaptic depression is age‐ and calcium‐dependent. J.Neurosci., 20: 5820–5826, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18. Komatsu Y., Age‐dependent long‐term potentiation of inhibitory synaptic transmission in rat visual cortex. J.Neurosci., 14: 6488–6499, 1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. McLean H.A., Caillard O., Ben‐Ari Y., Gaïarsa J.‐L., Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus, J.Physiol.(Lond.), 496: 471–477, 1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Gaïarsa J.L., Caillard O., Ben Ari Y., Long‐term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance, Trends Neurosci., 25: 564, 2002. [DOI] [PubMed] [Google Scholar]
  • 21. Caillard O., Ben‐Ari Y., Gaïarsa J.‐L., Long‐term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus, J.Physiol.(Lond.), 518: 109–119, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22. Komatsu Y., Iwakiri M., Long‐term modification of inhibitory synaptic transmission in developing visual cortex, Neuroreport, 4: 907–910, 1993. [DOI] [PubMed] [Google Scholar]
  • 23. Caillard O., Ben‐Ari Y., Gaïarsa J.‐L., Mechanisms of induction and expression of long‐term depression at GABAergic synapses in neonatal rat hippocampus, J. Neurosci., 19: 7568–7577, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24. Komatsu Y., GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate‐induced Ca2+ release are involved in the induction of long‐term potentiation at visual cortical inhibitory synapses, J. Neurosci., 16: 6342–6352, 1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Caillard O., Ben‐Ari Y., Gaïarsa J.‐L., Activation of presynaptic and postsynaptic ryanodine‐sensitive calcium stores is required for the induction of long‐term depression at GABAergic synapses in the neonatal rat hippocampus, J. Neurosci., 20: 1–5, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. Kang J., Jiang L., Goldman S.A., Nedergaard M., Kang J. Astrocyte‐mediated potentiation of inhibitory synaptic transmission. Nature Neuroscience, 1: 683–692, 1998. [DOI] [PubMed] [Google Scholar]
  • 27. Chevaleyre V., Castillo P.E., Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron, 38: 461–472, 2003. [DOI] [PubMed] [Google Scholar]
  • 28. Freund T., Buzsaki G., Interneurons of the hippocampus. Hippocampus, 6: 345–470, 1996. [DOI] [PubMed] [Google Scholar]
  • 29. Oda Y., Kawasaki H., Morita M., Korn H., Matsui H., Inhibitory long‐term potentiation underlies auditory conditioning of goldfish escape behaviour. Nature, 394: 182–185, 1998. [DOI] [PubMed] [Google Scholar]
  • 30. Korn H., Oda Y., Faber D.S., Long‐term potentiation of inhibitory circuits and synapses in the central nervous system. Proc.Natl.Acad.Sci.USA, 89: 440–443, 1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. Oda Y., Charpier S., Murayama Y., Suma C., Korn H., Long‐term potentiation of glycinergic inhibitory synaptic transmission. J. Neurophysiol., 74: 1056–1074, 1995. [DOI] [PubMed] [Google Scholar]
  • 32. Charpier S., Behrends J.C., Triller A., Faber D.S., Korn H., “Latent” inhibitory connections become functional during activity‐dependent plasticity, Proc. Natl. Acad. Sci.U.S.A., 92: 117–120, 1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. Gubellini P., Ben‐Ari Y., Gaïarsa J.‐L., Activity‐ and age‐dependent GABAergic synaptic plasticity in the developing rat hippocampus, Eur. J. Neurosci., 14: 1937–1946, 2001. [DOI] [PubMed] [Google Scholar]
  • 34. Leinekugel X., Khazipov R., Cannon R., Hirase H., Ben‐Ari Y., Buzsáki G., Correlated burst of activity in the neonatal rat hippocmpus in vivo , Science, 296: 2049–2052, 2002. [DOI] [PubMed] [Google Scholar]
  • 35. Menendez de la Prida L., Sanchez‐Andres J.V., Heterogenous populations of cells mediate spontaneous synchronous bursting in the developing hippocampus though a frequency‐dependent mechanism, Neuroscience, 97: 227–241, 2000. [DOI] [PubMed] [Google Scholar]
  • 36. Ben‐Ari Y., Cherubini E., Corradetti R., Gaïarsa J.‐L., Giant synaptic potentials in immature rat CA3 hippocampal neurones, J.Physiol.(Lond.), 416: 303–325, 1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37. Gaïarsa J.L., Caillard O., Ben Ari Y., Long‐term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance, Trends Neurosci., 25: 564, 2002. [DOI] [PubMed] [Google Scholar]
  • 38. Ben‐Ari Y., Khazipov R., Leinekugel X., Caillard O., Gaïarsa J.‐L., GABAA, NMDA and AMPA receptors: a developmentally regulated ‘ménage a trois’, Trends Neurosci., 20: 523–529, 1997. [DOI] [PubMed] [Google Scholar]
  • 39. Tyzio R., Represa A., Jorquera I., Ben‐Ari Y., Gozlan H., Aniksztejn L., The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci., 19: 10372–10382, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40. Hennou S., Khalilov I., Diabira D., Ben Ari Y., Gozlan H., Early sequential formation of functional GABAA and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur. J. Neurosci., 16: 197–208, 2002. [DOI] [PubMed] [Google Scholar]
  • 41. Seil F.J., Drake‐Baumann R., TrkB receptor ligands promote activity‐dependent inhibitory synaptogenesis. J. Neurosci., 20: 5367–5373, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Aguado F., Carmona M.A., Pozas E., Aguilo A., Martinez‐Guijarro F.J., Alcantara S., Borrell V., Yuste R., Ibanez C.F., Soriano E., BDNF regulates sponaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of K+/Cl‐ cotransport, Development, 130: 1287–1280, 2003. [DOI] [PubMed] [Google Scholar]
  • 43. Marty S., Berninger B., Carroll P., Thoenen H., GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brainderived neurotrophic factor, Neuron, 16: 565–570, 1996. [DOI] [PubMed] [Google Scholar]
  • 44. Vicario‐Abejon C., Collin C., McKay R.D., Segal M., Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci., 18: 7256–7271, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45. Schwyzer L., Mateos J.M., Abegg M., Rietschin L., Heeb L., Thompson S.M., Luthi A., Gahwiler B.H., McKinney R.A., Physiological and morphological plasticity induced by chronic treatment with NT‐3 or NT‐4/5 in hippocampal slice cultures, Eur. J. Neurosci., 16: 1939–1948, 2002. [DOI] [PubMed] [Google Scholar]
  • 46. Tanaka T., Saito H., Matsuki N., Inhibition of GABAA synaptic responses by brain‐derived neurotrophic factor (BDNF) in rat hippocampus, J. Neurosci., 17: 2959–2966, 1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Li Y.X., Zhang Y., Lester H.A., Schuman E.M., Davidson N. Enhanement of neurotransmitter release induced by brain‐derived neurotrophic factor in cultured hippoampal neurons. J. Neurosci., 18: 10231–10240, 1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48. MacLean Bolton M., Pittman A.J., Lo D.C., Brainderived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippoampal neurons, J.Neurosci., 20: 3221–3232, 2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Gao B.X., Van den Pol A.N., Neurotrophin‐3 potentiates GABAergic ynaptic transmission in cultured developing hypothalamic neurones of the rat, J. Physiol. (Lond.), 518: 81–95, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50. Kotak V.C., Dimattina C., Sanes D.H., GABAB and Trk receptor signaling mediates long‐lasting inhibitory synaptic depression., J. Neurophysiol., 86: 536–540, 2001. [DOI] [PubMed] [Google Scholar]
  • 51. Ben‐Ari Y., Developing networks play similar melody. Trends Neurosci., 24: 354–360, 2001. [DOI] [PubMed] [Google Scholar]

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