Long-Term Modification at Inhibitory Synapses in Developing Visual Cortex

Chapter

Abstract

Involvement of bidirectional modification at excitatory synapses in experience-dependent cortical maturation has been supported by various experimental data in visual cortex. Experiments using slice preparations demonstrated that cortical inhibitory synapses also undergo long-term potentiation (LTP) and depression (LTD) during the critical period. High-frequency stimulation (HFS) of excitatory and inhibitory inputs to pyramidal neurons induces LTD at inhibitory synapses when it elicits depolarizing responses large enough to activate NMDA receptors. HFS induces inhibitory LTP instead when it fails to activate NMDA receptors. Thus, the direction of modification is determined by postsynaptic NMDA receptors. LTD induction requires Ca2+ entry via NMDA receptors, whereas LTP induction requires IP3 receptor-mediated Ca2+ release, presumably triggered by GABAB receptor activation in the absence of substantial NMDA receptor activation. Intracellular Ca2+ release likely initiates BDNF release from the postsynaptic cell and activates TrkB receptors on inhibitory terminals, presumably leading to presynaptic enhancement of synaptic transmission. LTP maintenance requires presynaptic, but not postsynaptic, firing and associated Ca2+ entry at some intervals. This bidirectional modification at inhibitory synapses may contribute to the refinement and maintenance of visual responsiveness, and regulation of the critical period in visual cortex.

References

  1. Artola A, Bröcher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347: 69–72PubMedCrossRefGoogle Scholar
  2. Bear FM, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19: 437–462PubMedCrossRefGoogle Scholar
  3. Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237: 42–48PubMedCrossRefGoogle Scholar
  4. Bear MF, Kirkwood A (1993) Neocortical long-term potentiation, Curr Opin Neurobiol 3: 197–202PubMedCrossRefGoogle Scholar
  5. Castrén E, Zafra F, Thoenen H et al. (1992) Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc Natl Acad Sci USA 89: 9444–9448PubMedCrossRefGoogle Scholar
  6. Cellerino A, Maffei L, Domenici L (1996) The distribution of brain-derived neurotrophic factor and its receptor trkB in parvalbumin-containing neurons of the rat visual cortex. Eur J Neurosci 8: 1190–1197PubMedCrossRefGoogle Scholar
  7. Crawford MLA, Young JM (1990) Potentiation by γ-aminobutyric acid of α1-agonist-induced accumulation of inositol phosphates in slices of rat cerebral cortex. J Neurochem 54: 2100–2109PubMedCrossRefGoogle Scholar
  8. Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60: 1288–1294PubMedCrossRefGoogle Scholar
  9. Fawcett JP, Aloyz R, McLean JH et al. (1997) Detection of brain-derived neurotrophic factor in a vesicular fraction of brain synaptosomes. J Biol Chem 272: 8837–8840PubMedCrossRefGoogle Scholar
  10. Freeman RD, Mallach R, Hartley S (1981) Responsivity of normal kitten striate cortex deteriorates after brief binocular deprivation. J Neurophysiol 45: 1074–1084PubMedGoogle Scholar
  11. Frégnac Y, Imbert M (1984) Development of neuronal selectivity in primary visual cortex of cat, Physiol Rev 64: 325–434PubMedGoogle Scholar
  12. Frégnac Y, Shulz D, Thorpe S et al. (1988) A cellular analogue of visual cortical plasticity. Nature 333: 367–370PubMedCrossRefGoogle Scholar
  13. Gorba T, Wahle P (1999) Expression of trkB and trkC but BDNF mRNA in neurochemically identified interneurons in rat visual cortex in vivo and in organotypic cultures. Eur J Neurosci 11: 1179–1190PubMedCrossRefGoogle Scholar
  14. Gu Q, Singer W (1995) Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur J Neurosci 7: 1146–1153PubMedCrossRefGoogle Scholar
  15. Gubellini P, Ben-Ari Y, Gaïarsa J-L (2005) Endogenous neurotrophins are required for the induction of GABAergic long-term potentiation in the neonatal rat hippocampus. J Neurosci 25: 5796–5802PubMedCrossRefGoogle Scholar
  16. Gustafsson B, Wigström H, Abraham WC et al. (1987) Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci 7: 774–780PubMedGoogle Scholar
  17. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nature Rev Neurosci 6: 877–888CrossRefGoogle Scholar
  18. Heynen AJ, Yoon B-J, Liu C-H et al. (2003) Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 6: 854–862PubMedCrossRefGoogle Scholar
  19. Huang ZJ, Kirkwood A, Pizzorusso T et al. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98: 739–755PubMedCrossRefGoogle Scholar
  20. Inagaki T, Begum T, Reza F et al. (2008) Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons. Neurosci Res 61: 192–200PubMedCrossRefGoogle Scholar
  21. Itami C, Kimura F, Nakamura S (2007) Brain-derived neurotrophic factor regulates the maturation of layer 4 fast-spiking cells after the second postnatal week in the developing barrel cortex. J Neurosci 27: 2241–2252PubMedCrossRefGoogle Scholar
  22. Jin X, Hu H, Mathers PH et al. (2003) Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J Neurosci 23: 5662–5673PubMedGoogle Scholar
  23. Kasamatsu T, Pettigrew JD (1976) Depletion of brain catecholamine: failure of ocular dominance shift after monocular occlusion in kitten. Science 194: 206–209PubMedCrossRefGoogle Scholar
  24. Katoh-Semba R, Takeuchi IK, Semba R et al. (1997) Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 69: 34–42PubMedCrossRefGoogle Scholar
  25. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274: 1133–1138PubMedCrossRefGoogle Scholar
  26. Knüsel B, Hefti F (1992) K-252 compounds: modulators of neurotrophin signal transduction. J Neurochem 59: 1987–1996PubMedCrossRefGoogle Scholar
  27. Kohara K, Kitamura A, Adachi N et al. (2003) Inhibitory but not excitatory cortical neurons require presynaptic brain-derived neurotrophic factor for dendritic development, as revealed by chimera cell culture. J Neurosci 23: 6123–6131PubMedGoogle Scholar
  28. Kohara K, Yasuda H, Huang Y et al. (2007) A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. J Neurosci 27: 7234–7244PubMedCrossRefGoogle Scholar
  29. Komatsu Y (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J Neurosci 14: 6488–6499PubMedGoogle Scholar
  30. Komatsu Y (1996) 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: 6342–6352PubMedGoogle Scholar
  31. Komatsu Y, Iwakiri M (1993) Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport 4: 907–910PubMedCrossRefGoogle Scholar
  32. Komatsu Y, Yoshimura Y (2000) Activity-dependent maintenance of long-term potentiation at visual cortical inhibitory synapses. J Neurosci 20: 7539–7546PubMedGoogle Scholar
  33. Lessmann V, Gottmann K, Malcangio M (2003) Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69: 341–374PubMedCrossRefGoogle Scholar
  34. Lisman J (1994) The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17: 406–7546PubMedCrossRefGoogle Scholar
  35. Liu Y, Zhang LI, Tao HW (2007) Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J Neurosci 27: 5301–5312PubMedCrossRefGoogle Scholar
  36. Maffei A, Nataraj K, Nelson SB et al. (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443: 81–84PubMedCrossRefGoogle Scholar
  37. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16: 521–527PubMedCrossRefGoogle Scholar
  38. Malinow R, Miller JP (1986) Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320: 529–530PubMedCrossRefGoogle Scholar
  39. Manabe T, Wyllie DJA, Perkel DJ et al. (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neuophysiol 70: 1451–1459Google Scholar
  40. McLean HA, Caillard O, Ben-Ari Y et al. (1996) Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J Physiol Lond 496: 471–477PubMedGoogle Scholar
  41. Morales B, Choi S-Y, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22: 8084–8090PubMedGoogle Scholar
  42. Mower GD (1991) The effect of dark rearing on the time course of the critical period in cat visual cortex. Dev Brain Res 58: 151–158CrossRefGoogle Scholar
  43. Pollock GS, Vernon E, Forbes ME et al. (2001) Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J Neurosci 21: 3923–3931PubMedGoogle Scholar
  44. Reiter HO, Stryker MP (1988) Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. Proc Natl Acd Sci USA 85: 3623–3627CrossRefGoogle Scholar
  45. Rocamora N, Welker E, Pascual M et al. (1996) Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J Neurosci 16: 4411–4419PubMedGoogle Scholar
  46. Rutherford LC, DeWan A, Lauer HM et al. (1997) Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J Neurosci 17: 4527–4535PubMedGoogle Scholar
  47. Schoups AA, Elliott RC, Friedman WJ et al. (1995) NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Dev Brain Res 86: 326–334CrossRefGoogle Scholar
  48. Shelton DL, Sutherland J, Gripp J et al. (1995) Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J Neurosci 15: 477–491PubMedGoogle Scholar
  49. Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol Lond 250: 305–1975PubMedGoogle Scholar
  50. Singer W (1995) Development and plasticity of cortical processing architectures. Science 270: 758–764PubMedCrossRefGoogle Scholar
  51. Sompolinsky H, Shapley R (1997) New perspectives on the mechanisms for orientation selectivity. Curr Opin Neurobiol 7: 514–522PubMedCrossRefGoogle Scholar
  52. Stent G (1973) A physiological mechanism for Hebb’s postulate of learning. Proc Nat Acd Sci USA 70: 997–1001CrossRefGoogle Scholar
  53. Tao HW, Poo M-M (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45: 829–836PubMedCrossRefGoogle Scholar
  54. Tsumoto T (1992) Long-term potentiation and long-term depression in the neocortex. Prog Neurobiol 39: 209–228PubMedCrossRefGoogle Scholar
  55. Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299: 583–592PubMedCrossRefGoogle Scholar
  56. Yoshimura Y, Inaba M, Yamada K et al. (2008) Involvement of T-type Ca2+ channels in the potentiation of synaptic and visual responses during the critical period in rat visual cortex. Eur J Neurosci 28: 730–743PubMedCrossRefGoogle Scholar
  57. Yoshimura Y, Ohmura T, Komatsu Y (2003) Two forms of synaptic plasticity with distinct dependence on age, experience and NMDA receptor subtype in rat visual cortex. J Neurosci 23: 6557–6566PubMedGoogle Scholar
  58. Zhang LI, Poo M-M (2001) Electrical activity and development of neural circuits. Nat Neurosci Suppl 4: 1207–1214CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Neuroscience, Research Institute of Environmental MedicineNagoya UniversityNagoyaJapan

Personalised recommendations