Presynaptic gating of postsynaptically expressed plasticity at mature thalamocortical synapses

Journal of Neuroscience

Volumn 31, Issue 44, 2011, Pages 16012-16025

  Blundon, Jay A ^a   Bayazitov, Ildar T ^a   Zakharenko, Stanislav S ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A1 RECEPTOR; METABOTROPIC RECEPTOR 1; MUSCARINIC M1 RECEPTOR; NEUROTRANSMITTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BRAIN SLICE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DOWN REGULATION; FEMALE; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC GATING; PRIORITY JOURNAL; SYNAPSE; THALAMOCORTICAL TRACT; THALAMUS;

ANIMALS; CEREBRAL CORTEX; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMATES; INDOLES; ION CHANNEL GATING; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RECEPTOR, ADENOSINE A1; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 80155212418     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3281-11.2011     Document Type: Article

References (91)

1. Bakin JS, Weinberger NM (1996) Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A 93:11219-11224.
2. Beierlein M, Connors BW (2002) Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J Neurophysiol 88:1924-1932.
3. Blundon JA, Zakharenko SS (2008) Dissecting the components of longterm potentiation. Neuroscientist 14:598-608.
4. Bouron A, Reuter H (1997) Muscarinic stimulation of synaptic activity by protein kinase C is inhibited by adenosine in cultured hippocampal neurons. Proc Natl Acad Sci U S A 94:12224-12229.
5. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627.
6. Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Annu Rev Neurosci 21:149-186.
7. Carmignoto G, Vicini S (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007-1011.
8. Chang EF, Merzenich MM (2003) Environmental noise retards auditory cortical development. Science 300:498-502.
9. Choi SY, Chang J, Jiang B, Seol GH, Min SS, Han JS, Shin HS, Gallagher M, Kirkwood A (2005) Multiple receptors coupled to phospholipase C gate long-term depression in visual cortex. J Neurosci 25:11433-11443.
10. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299-1301.
11. Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459-473.
12. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
13. Cruikshank SJ, Rose HJ, Metherate R (2002) Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87:361-384.
14. Daw MI, Scott HL, Isaac JT (2007) Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol Cell Neurosci 34:493-502.
15. Daw NW, Fox K, Sato H, Czepita D (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67:197-202.
16. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27:180-189.
17. Dodt HU, Eder M, Schierloh A, Zieglgänsberger W (2002) Infrared-guided laser stimulation of neurons in brain slices. Sci STKE 2002:pl2.
18. Dorrn AL, Yuan K, Barker AJ, Schreiner CE, Froemke RC (2010) Developmental sensory experience balances cortical excitation and inhibition. Nature 465:932-936.
19. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22:567-631.
20. Dringenberg HC, Hamze B, Wilson A, Speechley W, Kuo MC (2007) Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb Cortex 17:839-848.
21. Dudek SM, Friedlander MJ (1996) Developmental down-regulation of LTD in cortical layer IV and its independence of modulation by inhibition. Neuron 16:1097-1106.
22. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31-55.
23. Dunwiddie TV, Hoffer BJ, Fredholm BB (1981) Alkylxanthines elevate hippocampal excitability. Evidence for a role of endogenous adenosine. Naunyn Schmiedebergs Arch Pharmacol 316:326-330.
24. Earls LR, Bayazitov IT, Fricke RG, Berry RB, Illingworth E, Mittleman G, Zakharenko SS (2010) Dysregulation of presynaptic calcium and synaptic plasticity in a mouse model of 22q11 deletion syndrome. J Neurosci 30:15843-15855.
25. Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310:810-815.
26. Feldman DE, Nicoll RA, Malenka RC, Isaac JT (1998) Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 21:347-357.
27. Feldman DE, Nicoll RA, Malenka RC (1999) Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J Neurobiol 41:92-101.
28. Feldman ML, Peters A (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J Comp Neurol 179:761-793.
29. Foeller E, Feldman DE (2004) Synaptic basis for developmental plasticity in somatosensory cortex. Curr Opin Neurobiol 14:89-95.
30. Fox K (2002) Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111:799-814.
31. Fritz JB, Elhilali M, David SV, Shamma SA (2007) Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? Hear Res 229:186-203.
32. Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450:425-429.
33. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
34. Gilbert CD (1998) Adult cortical dynamics. Physiol Rev 78:467-485.
35. Grover LM, Teyler TJ (1993) Role of adenosine in heterosynaptic, posttetanic depression in area CA1 of hippocampus. Neurosci Lett 154:39-42.
36. Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351-359.
37. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877-888.
38. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508.
39. Heynen AJ, Bear MF (2001) Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo. J Neurosci 21:9801-9813.
40. Hirata A, Castro-Alamancos MA (2006) Relief of synaptic depression produces long-term enhancement in thalamocortical networks. J Neurophysiol 95:2479-2491.
41. Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419-436.
42. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
43. - conductance. Neurosci Res 6: 72-75.
44. Isaac JT, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
45. Jiang B, Treviño M, Kirkwood A (2007) Sequential development of longterm potentiation and depression in different layers of the mouse visual cortex. J Neurosci 27:9648-9652.
46. Jo J, Son GH, Winters BL, Kim MJ, Whitcomb DJ, Dickinson BA, Lee YB, Futai K, Amici M, Sheng M, Collingridge GL, Cho K (2010) Muscarinic receptors induce LTD of NMDAR EPSCs via a mechanism involving hippocalcin, AP2 and PSD-95. Nat Neurosci 13:1216-1224.
47. Johansson B, Halldner L, Dunwiddie TV, Masino SA, Poelchen W, Giménez-Llort L, Escorihuela RM, Fernández-Teruel A, Wiesenfeld-Hallin Z, Xu XJ, Hårdemark A, Betsholtz C, Herlenius E, Fredholm BB (2001) Hy-peralgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci U S A 98:9407-9412.
48. Kamsler A, McHugh TJ, Gerber D, Huang SY, Tonegawa S (2010) Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus. Proc Natl Acad Sci U S A 107:1618-1623.
49. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
50. Kemp N, Bashir ZI (1999) Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors. Neuropharmacology 38:495-504.
51. Kemp N, McQueen J, Faulkes S, Bashir ZI (2000) Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 12:360-366.
52. Keuroghlian AS, Knudsen EI (2007) Adaptive auditory plasticity in developing and adult animals. Prog Neurobiol 82:109-121.
53. Kilgard MP, Merzenich MM (1998a) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714-1718.
54. Kilgard MP, Merzenich MM (1998b) Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci 1:727-731.
55. Kirkwood A, Bear MF (1994) Hebbian synapses in visual cortex. J Neurosci 14:1634-1645.
56. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF (1999) Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19:1599-1609.
57. Lee CC, Sherman SM (2008) Synaptic properties of thalamic and intracortical inputs to layer 4 of the first-and higher-order cortical areas in the auditory and somatosensory systems. J Neurophysiol 100:317-326.
58. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10:1594-1600.
59. Lund JS (1973) Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 147:455-496.
60. Ma X, Suga N (2005) Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci U S A 102:9335-9340.
61. MacLean JN, Fenstermaker V, Watson BO, Yuste R (2006) A visual thalamocortical slice. Nat Methods 3:129-134.
62. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
63. Malenka RC, Madison DV, Nicoll RA (1986) Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 321:175-177.
64. Manzoni OJ, Manabe T, Nicoll RA (1994) Release of adenosine by activation of NMDA receptors in the hippocampus. Science 265:2098-2101.
65. Mateo Z, Porter JT (2007) Group II metabotropic glutamate receptors inhibit glutamate release at thalamocortical synapses in the developing somatosensory cortex. Neuroscience 146:1062-1072.
66. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
67. Metherate R, Ashe JH (1993) Ionic flux contributions to neocortical slow waves and nucleus basalis-mediated activation: whole-cell recordings in vivo. J Neurosci 13:5312-5323.
68. Mitchell JB, Lupica CR, Dunwiddie TV (1993) Activity-dependent release of endogenous adenosine modulates synaptic responses in the rat hippocampus. J Neurosci 13:3439-3447.
69. Morishita H, Miwa JM, Heintz N, Hensch TK (2010) Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330:1238-1240.
70. Nelson S, Toth L, Sheth B, Sur M (1994) Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265:774-777.
71. Nicholls DG (1995) Proteins, transmitters and synapses. Oxford: Blackwell.
72. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
73. Oliveira L, Timóteo MA, Correia-de-Sá P (2009) Negative crosstalk betweenM1 andM2 muscarinic autoreceptors involves endogenous adenosine activating A1 receptors at the rat motor endplate. Neurosci Lett 459:127-131.
74. Richardson RJ, Blundon JA, Bayazitov IT, Zakharenko SS (2009) Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J Neurosci 29:6406-6417.
75. Rose HJ, Metherate R (2005) Auditory thalamocortical transmission is reliable and temporally precise. J Neurophysiol 94:2019-2030.
76. Shapira R, Silberberg SD, Ginsburg S, Rahamimoff R (1987) Activation of protein kinaseCaugments evoked transmitter release. Nature 325:58-60.
77. Smith PH, Populin LC (2001) Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J Comp Neurol 436:508-519.
78. Stratford KJ, Tarczy-Hornoch K, Martin KA, Bannister NJ, Jack JJ (1996) Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382:258-261.
79. Tallal P, Benasich AA (2002) Developmental language learning impairments. Dev Psychopathol 14:559-579.
80. Volk LJ, Pfeiffer BE, Gibson JR, Huber KM (2007) Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 27:11624-11634.
81. Weinberger NM (2004) Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5:279-290.
82. Weinberger NM (2007a) Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn Mem 14:1-16.
83. Weinberger NM (2007b) Auditory associative memory and representational plasticity in the primary auditory cortex. Hear Res 229:54-68.
84. Wimmer VC, Broser PJ, Kuner T, Bruno RM (2010) Experience-induced plasticity of thalamocortical axons in both juveniles and adults. J Comp Neurol 518:4629-4648.
85. Worley PF, Baraban JM, McCarren M, Snyder SH, Alger BE (1987) Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked neurotransmitter actions: electrophysiological studies in rat hippocampus. Proc Natl Acad Sci U S A 84:3467-3471.
86. 2+ channels by adenosine autoreceptors. Nature 365:256-258.
87. Yazaki-Sugiyama Y, Kang S, Câteau H, Fukai T, Hensch TK (2009) Bidirectional plasticity in fast-spikingGABAcircuits by visual experience. Nature 462:218-221.
88. Zakharenko SS, Zablow L, Siegelbaum SA (2001) Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4:711-717.
89. Zakharenko SS, Zablow L, Siegelbaum SA (2002) Altered presynaptic vesicle release and cycling diring mGluR-dependent LTD. Neuron 35:1099-1110.
90. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER, Morozov A (2003) PresynapticBDNFrequired for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39:975-990.
91. Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4:1123-1130.