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Excitatory-Inhibitory Balance Controls Critical Period Plasticity

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Excitatory-Inhibitory Balance

Abstract

Neuronal circuits are shaped by their activity during ‘critical’ or ‘sensitive periods’ in development. Initially spontaneous, then early sensory-evoked patterns of action potentials, are required to sculpt the remarkably complex connectivity found in the adult brain, which then loses this extraordinary level of plasticity. Whether it is the targeting of individual axons or the acquisition of language, there is no doubt that dramatic re-wiring is most powerful early in postnatal life. Despite decades of similar robust observations across a wide spectrum of brain functions, only recently have we begun to understand the cellular basis that may underlie this fundamental process. The ability to freely switch on or off critical period mechanisms confirms the very existence of such special stages of heightened plasticity. In this chapter, we will focus on a newfound perspective of excitatory-inhibitory balance within cortical circuits that has finally granted us this control.

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References

  1. Wiesel TN, Hubel DH. (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017.

    PubMed  CAS  Google Scholar 

  2. Daw N. (1995) Visual Development (Plenum, New York).

    Google Scholar 

  3. Trachtenberg JT, Stryker MP. (2001) Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J Neurosci. 21, 3476–3482.

    PubMed  CAS  Google Scholar 

  4. Antonini A, Stryker MP. (1993) Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819–1821.

    Article  PubMed  CAS  Google Scholar 

  5. Antonini A, Stryker MP. (1998) Effect of sensory disuse on geniculate afferents to cat visual cortex. Vis. Neurosci. 15, 401–409.

    Article  PubMed  CAS  Google Scholar 

  6. Hubel DH, Wiesel TN. (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond) 206, 419–436.

    CAS  Google Scholar 

  7. Berardi N, Pizzorusso T, Maffei L. (2000) Critical periods during sensory development. Curr. Opin. Neurobiol. 10, 138–145.

    Article  PubMed  CAS  Google Scholar 

  8. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L. (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 34, 709–720.

    Article  PubMed  CAS  Google Scholar 

  9. Gordon JA, Stryker MP. (1996) Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci. 16, 3274–3286.

    PubMed  CAS  Google Scholar 

  10. Cynader M. (1983) Prolonged sensitivity to monocular deprivation in dark-reared cats: effects of age and visual exposure. Brain Res. 284, 155–164.

    PubMed  CAS  Google Scholar 

  11. 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 

  12. Benevento LA, Bakkum BW, Port JD, Cohen RS. (1992) The effects of dark-rearing on the electrophysiology of the rat visual cortex. Brain Res. 572, 198–207.

    Article  PubMed  CAS  Google Scholar 

  13. Fagiolini M et al. (2003) Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proc. Natl. Acad. Sci. USA 100, 2854–2859.

    Article  PubMed  CAS  Google Scholar 

  14. Prusky GT, Douglas RM. (2003) Developmental plasticity of mouse visual acuity. Eur. J. Neurosci. 17, 167–173.

    Article  PubMed  Google Scholar 

  15. Antonini A, Fagiolini M, Stryker MP. (1999) Anatomical correlates of functional plasticity in mouse visual cortex. J Neurosci. 19, 4388–4406.

    PubMed  CAS  Google Scholar 

  16. Sanes JR, Lichtman JW. (1999) Can molecules explain long-term potentiation? Nat. Neurosci. 2, 597–604.

    Article  PubMed  CAS  Google Scholar 

  17. Hensch TK, Stryker MP. (1996) Ocular dominance plasticity under metabotropic glutamate receptor blockade. Science 272, 554–557

    Article  PubMed  CAS  Google Scholar 

  18. Gordon JA, Cioffi D, Silva AJ, Stryker MP. (1996) Deficient plasticity in the primary visual cortex of alpha-calcium/calmodulin-dependent protein kinase II mutant mice. Neuron. 17, 491–499.

    Article  PubMed  CAS  Google Scholar 

  19. Kirkwood A, Silva A, Bear MF. (1997) Age-dependent decrease of synaptic plasticity in the neocortex of alphaCaMKII mutant mice. Proc. Natl. Acad. Sci. USA 94, 3380–3383.

    Article  PubMed  CAS  Google Scholar 

  20. Hensch TK et al. (1998) Comparison of plasticity in vivo and in vitro in the developing visual cortex of normal and protein kinase A RIbeta-deficient mice. J. Neurosci. 18, 2108–2117.

    PubMed  CAS  Google Scholar 

  21. Renger JJ et al. (2002) Experience-dependent plasticity without long-term depression by type 2 metabotropic glutamate receptors in developing visual cortex.Proc. Natl. Acad. Sci. USA 99, 1041–1046.

    Article  PubMed  CAS  Google Scholar 

  22. Bartoletti A et al. (2002) Heterozygous knock-out mice for brain-derived neurotrophic factor show a pathway-specific impairment of long-term potentiation but normal critical period for monocular deprivation. J Neurosci .22, 10072–10077.

    PubMed  CAS  Google Scholar 

  23. Jiang B, Akaneya Y, Hata Y, Tsumoto T. (2003) Long-term depression is not induced by low-frequency stimulation in rat visual cortex in vivo: a possible preventing role of endogenous brain-derived neurotrophic factor. J Neurosci. 23, 3761–3770.

    PubMed  CAS  Google Scholar 

  24. Hensch TK. (2003) Controlling the critical period. Neurosci. Res., in press.

    Google Scholar 

  25. Ramoa AS, Paradiso MA, Freeman RD. (1988) Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity. Exp. Brain Res. 73, 285–296.

    Article  PubMed  CAS  Google Scholar 

  26. Videen TO, Daw NW, Collins RC. ( 1986 ) Penicillin-induced epileptiform activity does not prevent ocular dominance shifts in monocularly deprived kittens. Brain Res. 371, 1–8.

    Article  PubMed  CAS  Google Scholar 

  27. Shaw C, Cynader M. (1984) Disruption of cortical activity prevents ocular dominance changes in monocularly deprived kittens. Nature 308, 731–734.

    Article  PubMed  CAS  Google Scholar 

  28. 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. Acad. Sci. USA. 85, 3623–3627.

    Article  PubMed  CAS  Google Scholar 

  29. Soghomonian JJ, Martin DL (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol. 19, 500–505.

    Article  CAS  Google Scholar 

  30. Asada H et al. (1997) Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94, 6496–6499.

    Article  PubMed  CAS  Google Scholar 

  31. Asada H et al. (1996) Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem. Biophys. Res. Commun. 229, 891–895.

    Article  PubMed  CAS  Google Scholar 

  32. Kash SF et al. (1997) Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad Sci. USA 94, 14060–14065

    Article  PubMed  CAS  Google Scholar 

  33. Hensch TK et al. (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508.

    Article  PubMed  CAS  Google Scholar 

  34. Tian N et al. (1999) The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc. Natl. Acad. Sci. USA 96, 12911–12916.

    Article  PubMed  CAS  Google Scholar 

  35. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H. (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci. 17, 2469–2476.

    PubMed  CAS  Google Scholar 

  36. Nase G, Weishaupt J, Stern P, Singer W, Monyer H. ( 1999 ) Genetic and epigenetic regulation of NMDA receptor expression in the rat visual cortex. Eur. J. Neurosci..11, 4320–4326.

    Article  PubMed  CAS  Google Scholar 

  37. Miller KD, Chapman B, Stryker MP. (1989) Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA. 86, 5183–5187.

    Article  PubMed  CAS  Google Scholar 

  38. Cherubini E, Conti F. (2001) Generating diversity at GABAergic synapses. Trends Neurosci. 24, 155–162.

    Article  PubMed  CAS  Google Scholar 

  39. Eghbali M, Curmi JP, Birnir B, Gage PW. (1997) Hippocampal GABAA channel conductance increased by diazepam. Nature 388, 71–75.

    Article  PubMed  CAS  Google Scholar 

  40. Sieghart W. (1995) Structure and pharmacology of γ-aminobutyric acidA receptor subtypes. Pharmacol. Rev. 47, 181–234.

    PubMed  CAS  Google Scholar 

  41. Shaw C, Aoki C, Wilkinson M, Prusky G, Cynader M. (1987) Benzodiazepine ([3H]flunitrazepam) binding in cat visual cortex: ontogenesis of normal characteristics and the effects of dark rearing. Brain Res. 465, 67–76.

    PubMed  CAS  Google Scholar 

  42. Fagiolini M, Hensch TK. (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404, 183–186.

    Article  PubMed  CAS  Google Scholar 

  43. Bi G, Poo M. (2001) Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu. Rev. Neurosci. 24, 139–166.

    Article  PubMed  CAS  Google Scholar 

  44. del Cerro S, Jung M, Lynch G. ( 1992 ) Benzodiazepines block long-term potentiation in slices of hippocampus and pyriform cortex. Neuroscience 49, 1–6.

    Article  PubMed  Google Scholar 

  45. Trepel C, Racine RJ. (2000) GABAergic modulation of neocortical long-term potentiation in the freely moving rat. Synapse 35, 120–128.

    Article  PubMed  CAS  Google Scholar 

  46. Fox, K. (1995) The critical period for long-term potentiation in primary sensory cortex. Neuron. 15, 485–488.

    Article  PubMed  CAS  Google Scholar 

  47. Miller, KD. (1996) Synaptic economics: competition and cooperation in synaptic plasticity. Neuron. 17, 371–374.

    Article  PubMed  CAS  Google Scholar 

  48. Song S, Miller KD, Abbott LF. (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3, 919–926.

    Article  PubMed  CAS  Google Scholar 

  49. Feldman DE. (2000) Inhibition and plasticity. Nat. Neurosci. 3, 303–304.

    Article  PubMed  CAS  Google Scholar 

  50. Pouille F, Scanziani M. (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibtion. Science 293, 1159–1163.

    Article  PubMed  CAS  Google Scholar 

  51. DeFelipe, J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 14, 1–19 (1997).

    Article  PubMed  CAS  Google Scholar 

  52. Somogyi P, Tamas G, Lujan R, Buhl EH. (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26, 113–135.

    Article  PubMed  CAS  Google Scholar 

  53. Rudy B, McBain CJ. (2001) Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci. 24, 517–526.

    Article  PubMed  CAS  Google Scholar 

  54. Erisir A, Lau D, Rudy B, Leonard CS. (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J. Neurophysiol. 82, 2476–2489.

    PubMed  CAS  Google Scholar 

  55. Lien CC, Jonas P. (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci. 23, 2058–2068.

    PubMed  CAS  Google Scholar 

  56. Klausberger T, Roberts JD, Somogyi P. (2002) Cell type- and input-specific differences in the number and subtypes of synaptic GABA(A) receptors in the hippocampus. J Neurosci. 22, 2513–2521.

    PubMed  CAS  Google Scholar 

  57. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P. (1996) Differential synaptic localization of two major gamma- aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93, 11939–11944.

    Article  PubMed  CAS  Google Scholar 

  58. Rudolph U, Crestani F, Mohler H. (2001) GABA(A) receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci. 22, 188–194.

    Article  PubMed  CAS  Google Scholar 

  59. Buzas P, Eysel UT, Adorjan P, Kisvarday ZF. (2001) Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps. J. Comp. Neurol. 437, 259–285.

    Article  PubMed  CAS  Google Scholar 

  60. Feldman DE, Knudsen EI. (1998) Experience-dependent plasticity and the maturation of glutamatergic synapses. Neuron. 20, 1067–1071.

    Article  PubMed  CAS  Google Scholar 

  61. Del Rio JA, De Lecea L, Ferrer I, Soriano E. (1994) The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Dev. Brain Res. 81, 247–259

    Article  Google Scholar 

  62. Huang ZJ et al. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739–755.

    Article  PubMed  CAS  Google Scholar 

  63. Hartig W et al. (1999) Cortical neurons immunoreactive for the potassium channel Kv3. lb subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res. 842, 15–29.

    Article  PubMed  CAS  Google Scholar 

  64. Pizzorusso T et al. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251.

    Article  PubMed  CAS  Google Scholar 

  65. Grutzendler J, Kasthuri N, Gan WB. (2002) Long-term dendritic spine stability in the adult cortex. Nature 420, 812–816.

    Article  PubMed  CAS  Google Scholar 

  66. Knott GW, Quairiaux C, Genoud C, Welker E. (2002) Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265–273.

    Article  PubMed  CAS  Google Scholar 

  67. Iwai Y, Fagiolini M, Obata K, Hensch TK. (2003) Rapid critical period induction by tonic inhibition in mouse visual cortex. J. Neurosci., in press.

    Google Scholar 

  68. Mataga N, Nagai N, Hensch TK. (2002) Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA 99, 7717–7721.

    Article  PubMed  CAS  Google Scholar 

  69. Morales B, Choi SY, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci. 22, 8084–8090.

    PubMed  CAS  Google Scholar 

  70. Sakaguchi H. (1996) Sex differences in the developmental changes of GABAergic neurons in zebra finch song control nuclei. Exp. Brain Res. 108, 62–68.

    Article  PubMed  CAS  Google Scholar 

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Fagiolini, M., Hensch, T.K. (2003). Excitatory-Inhibitory Balance Controls Critical Period Plasticity. In: Hensch, T.K., Fagiolini, M. (eds) Excitatory-Inhibitory Balance. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0039-1_18

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  • DOI: https://doi.org/10.1007/978-1-4615-0039-1_18

  • Publisher Name: Springer, Boston, MA

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