Skip to main content
SpringerLink
Log in

Long-Term Modification at Inhibitory Synapses in Developing Visual Cortex

  • Chapter
  • First Online:
Inhibitory Synaptic Plasticity

  • 616 Accesses

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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: 69–72

    Article  CAS  PubMed  Google Scholar 

  • Bear FM, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19: 437–462

    Article  CAS  PubMed  Google Scholar 

  • Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237: 42–48

    Article  CAS  PubMed  Google Scholar 

  • Bear MF, Kirkwood A (1993) Neocortical long-term potentiation, Curr Opin Neurobiol 3: 197–202

    Article  CAS  PubMed  Google Scholar 

  • 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: 9444–9448

    Article  PubMed  Google Scholar 

  • 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: 1190–1197

    Article  CAS  PubMed  Google Scholar 

  • 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: 2100–2109

    Article  CAS  PubMed  Google Scholar 

  • Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60: 1288–1294

    Article  CAS  PubMed  Google Scholar 

  • 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: 8837–8840

    Article  CAS  PubMed  Google Scholar 

  • Freeman RD, Mallach R, Hartley S (1981) Responsivity of normal kitten striate cortex deteriorates after brief binocular deprivation. J Neurophysiol 45: 1074–1084

    CAS  PubMed  Google Scholar 

  • Frégnac Y, Imbert M (1984) Development of neuronal selectivity in primary visual cortex of cat, Physiol Rev 64: 325–434

    PubMed  Google Scholar 

  • Frégnac Y, Shulz D, Thorpe S et al. (1988) A cellular analogue of visual cortical plasticity. Nature 333: 367–370

    Article  PubMed  Google Scholar 

  • 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: 1179–1190

    Article  CAS  PubMed  Google Scholar 

  • Gu Q, Singer W (1995) Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur J Neurosci 7: 1146–1153

    Article  CAS  PubMed  Google Scholar 

  • 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: 5796–5802

    Article  CAS  PubMed  Google Scholar 

  • 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: 774–780

    CAS  PubMed  Google Scholar 

  • Hensch TK (2005) Critical period plasticity in local cortical circuits. Nature Rev Neurosci 6: 877–888

    Article  CAS  Google Scholar 

  • 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: 854–862

    Article  CAS  PubMed  Google Scholar 

  • 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: 739–755

    Article  CAS  PubMed  Google Scholar 

  • 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: 192–200

    Article  CAS  PubMed  Google Scholar 

  • 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: 2241–2252

    Article  CAS  PubMed  Google Scholar 

  • 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: 5662–5673

    CAS  PubMed  Google Scholar 

  • Kasamatsu T, Pettigrew JD (1976) Depletion of brain catecholamine: failure of ocular dominance shift after monocular occlusion in kitten. Science 194: 206–209

    Article  CAS  PubMed  Google Scholar 

  • 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: 34–42

    Article  CAS  PubMed  Google Scholar 

  • Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274: 1133–1138

    Article  CAS  PubMed  Google Scholar 

  • Knüsel B, Hefti F (1992) K-252 compounds: modulators of neurotrophin signal transduction. J Neurochem 59: 1987–1996

    Article  PubMed  Google Scholar 

  • 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: 6123–6131

    CAS  PubMed  Google Scholar 

  • 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: 7234–7244

    Article  CAS  PubMed  Google Scholar 

  • Komatsu Y (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J Neurosci 14: 6488–6499

    CAS  PubMed  Google Scholar 

  • 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: 6342–6352

    CAS  PubMed  Google Scholar 

  • Komatsu Y, Iwakiri M (1993) Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport 4: 907–910

    Article  CAS  PubMed  Google Scholar 

  • Komatsu Y, Yoshimura Y (2000) Activity-dependent maintenance of long-term potentiation at visual cortical inhibitory synapses. J Neurosci 20: 7539–7546

    CAS  PubMed  Google Scholar 

  • Lessmann V, Gottmann K, Malcangio M (2003) Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69: 341–374

    Article  CAS  PubMed  Google Scholar 

  • Lisman J (1994) The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17: 406–7546

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang LI, Tao HW (2007) Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J Neurosci 27: 5301–5312

    Article  CAS  PubMed  Google Scholar 

  • Maffei A, Nataraj K, Nelson SB et al. (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443: 81–84

    Article  CAS  PubMed  Google Scholar 

  • Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16: 521–527

    Article  CAS  PubMed  Google Scholar 

  • Malinow R, Miller JP (1986) Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320: 529–530

    Article  CAS  PubMed  Google Scholar 

  • 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: 1451–1459

    CAS  Google Scholar 

  • 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: 471–477

    CAS  PubMed  Google Scholar 

  • Morales B, Choi S-Y, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22: 8084–8090

    CAS  PubMed  Google Scholar 

  • Mower GD (1991) The effect of dark rearing on the time course of the critical period in cat visual cortex. Dev Brain Res 58: 151–158

    Article  CAS  Google Scholar 

  • 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: 3923–3931

    CAS  PubMed  Google Scholar 

  • 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: 3623–3627

    Article  CAS  Google Scholar 

  • 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: 4411–4419

    CAS  PubMed  Google Scholar 

  • 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: 4527–4535

    CAS  PubMed  Google Scholar 

  • 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: 326–334

    Article  CAS  Google Scholar 

  • Shelton DL, Sutherland J, Gripp J et al. (1995) Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J Neurosci 15: 477–491

    CAS  PubMed  Google Scholar 

  • 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: 305–1975

    CAS  PubMed  Google Scholar 

  • Singer W (1995) Development and plasticity of cortical processing architectures. Science 270: 758–764

    Article  CAS  PubMed  Google Scholar 

  • Sompolinsky H, Shapley R (1997) New perspectives on the mechanisms for orientation selectivity. Curr Opin Neurobiol 7: 514–522

    Article  CAS  PubMed  Google Scholar 

  • Stent G (1973) A physiological mechanism for Hebb’s postulate of learning. Proc Nat Acd Sci USA 70: 997–1001

    Article  CAS  Google Scholar 

  • Tao HW, Poo M-M (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45: 829–836

    Article  CAS  PubMed  Google Scholar 

  • Tsumoto T (1992) Long-term potentiation and long-term depression in the neocortex. Prog Neurobiol 39: 209–228

    Article  CAS  PubMed  Google Scholar 

  • Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299: 583–592

    Article  CAS  PubMed  Google Scholar 

  • 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: 730–743

    Article  PubMed  Google Scholar 

  • 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: 6557–6566

    CAS  PubMed  Google Scholar 

  • Zhang LI, Poo M-M (2001) Electrical activity and development of neural circuits. Nat Neurosci Suppl 4: 1207–1214

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Research Institute of Environmental Medicine, Nagoya University, Nagoya, 464-8601, Japan

    Yukio Komatsu

Authors
  1. Yukio Komatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yumiko Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yukio Komatsu .

Editor information

Editors and Affiliations

  1. Dept. Cell & Systems Biology, Ramsay Wright Zoological Lab., University of Toronto, Harbord Street 25, Toronto, M5S 3G5, Ontario, Canada

    Melanie A. Woodin

  2. Stony Brook, Dept. Neurobiology & Behavior, State University of New York, Stony Brook, 11794-5230, New York, USA

    Arianna Maffei

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Komatsu, Y., Yoshimura, Y. (2011). Long-Term Modification at Inhibitory Synapses in Developing Visual Cortex. In: Woodin, M., Maffei, A. (eds) Inhibitory Synaptic Plasticity. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6978-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation