Role of efficient neurotransmitter release in barrel map development

Journal of Neuroscience

Volumn 26, Issue 10, 2006, Pages 2692-2703

  Lu, Hui Chen ^a   Butts, Daniel A ^b   Kaeser, Pascal S ^c   She, Wei Chi ^a   Janz, Roger ^d   Crair, Michael C ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Barrels; cAMP; Cortical map; Neurotransmitter release; PKA; Short term plasticity; Somatosensory

Indexed keywords

ADENYLATE CYCLASE; CALCIUM; DIZOCILPINE; NEUROTRANSMITTER; RAB PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; DEVELOPMENT; GENE; GENOTYPE; IMMUNOBLOTTING; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT;

ADENYLATE CYCLASE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN MAPPING; CALCIUM; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP-BINDING PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MODELS, NEUROLOGICAL; N-METHYLASPARTATE; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; SOMATOSENSORY CORTEX; SYNAPSINS; THALAMUS; TIME FACTORS;

EID: 33644817412     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3956-05.2006     Document Type: Article

References (86)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci [Suppl] 3:1178-1183.
2. Abdel-Majid RM, Leong WL, Schalkwyk LC, Smallman DS, Wong ST, Storm DR, Fine A, Dobson MJ, Guernsey DL, Neumann PE (1998) Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex. Nat Genet 19:289-291.
3. Agmon A, Yang LT, Jones EG, O'Dowd DK (1995) Topological precision in the thalamic projection to neonatal mouse barrel cortex. J Neurosci 15:549-561.
4. Amitai Y (2001) Thalamocortical synaptic connections: efficacy, modulation, inhibition and plasticity. Rev Neurosci 12:159-173.
5. Boczan J, Leenders AG, ShengZH (2004) Phosphorylation of syntaphilin by cAMP-dependent protein kinase modulates its interaction with syntaxin-1 and annuls its inhibitory effect on vesicle exocytosis. J Biol Chem 279:18911-18919.
6. Calakos N, Schoch S, Sudhof TC, Malenka RC (2004) Multiple roles for the active zone protein RIM1alpha in late stages of neurotransmitter release. Neuron 42:889-896.
7. Castillo PE, Schoch S, Schmitz F, Sudhof TC, Malenka RC (2002) RIM1alpha is required for presynaptic long-term potentiation. Nature 415:327-330.
8. Chandrasekaran AR, Plas DT, Gonzalez E, CrairMC (2005) Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J Neurosci 25:6929-6938.
9. Chen C, Blitz DM, Regehr WG (2002) Contributions of receptor desensitization and saturation to plasticity at the retinogeniculate synapse. Neuron 33:779-788.
10. Chheda MG, Ashery U, Thakur P, Rettig J, Sheng ZH (2001) Phosphorylation of Snapin by PKA modulates its interaction with the SNARE complex. Nat Cell Biol 3:331-338.
11. Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193.
12. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34:437-446.
13. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
14. Czernik AJ, Pang DT, Greengard P (1987) Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I. Proc Natl Acad Sci USA 84:7518-7522.
15. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23-30.
16. Datwani A, Iwasato T, Itohara S, Erzurumlu RS (2002) NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dendritic differentiation in the barrel cortex. Mol Cell Neurosci 21:477-492.
17. Dodge Jr FA, Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond) 193:419-432.
18. Erzurumlu RS, Kind PC (2001) Neural activity: sculptor of "barrels" in the neocortex. Trends Neurosci 24:589-595.
19. Evans GJ, Wilkinson MC, Graham ME, Turner KM, Chamberlain LH, Burgoyne RD, Morgan A (2001) Phosphorylation of cysteine string protein by protein kinase A. Implications for the modulation of exocytosis. J Biol Chem 276:47877-47885.
20. Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45-56.
21. Feng J, Chi P, Blanpied TA, Xu Y, Magarinos AM, Ferreira A, Takahashi RH, Kao HT, McEwen BS, Ryan TA, Augustine GJ, Greengard P (2002) Regulation of neurotransmitter release by synapsin III. J Neurosci 22:4372-4380.
22. Foeller E, Feldman DE (2004) Synaptic basis for developmental plasticity in somatosensory cortex. Curr Opin Neurobiol 14:89-95.
23. Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071-1074.
24. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
25. Greengard P (1987) Neuronal phosphoproteins. Mediators of signal transduction. Mol Neurobiol 1:81-119.
26. Hannan AJ, Blakemore C, Katsnelson A, Vitalis T, Huber KM, Bear M, Roder J, Kim D, Shin HS, Kind PC (2001) PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat Neurosci 4:282-288.
27. Harms KJ, Tovar KR, Craig AM (2005) Synapse-specific regulation of AMPA receptor subunit composition by activity. J Neurosci 25:6379-6388.
28. Hepp R, Cabaniols JP, Roche PA (2002) Differential phosphorylation of SNAP-25 in vivo by protein kinase C and protein kinase A. FEBS Lett 532:52-56.
29. Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366:569-572.
30. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
31. Hosaka M, Hammer RE, Sudhof TC (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24:377-387.
32. Hua JY, Smear MC, Baier H, Smith SJ (2005) Regulation of axon growth in vivo by activity-based competition. Nature 434:1022-1026.
33. Iwasaki S, Takahashi T (2001) Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol (Lond) 534:861-871.
34. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knopfel T, Erzurumlu RS, Itohara S (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406:726-731.
35. 2+-dependent glutamate release in isolated nerve terminals. J Neurosci 21:7944-7953.
36. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
37. Kidd FL, Isaac JT (1999) Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400:569-573.
38. Killackey HP, Leshin S (1975) The organization of specific thalamocortical projections to the posteromedial barrel subfield of the rat somatic sensory cortex. Brain Res 86:469-472.
39. Lao G, Scheuss V, Gerwin CM, Su Q, Mochida S, Rettig J, Sheng ZH (2000) Syntaphilin: a syntaxin-1 clamp that controls SNARE assembly. Neuron 25:191-201.
40. Lee LJ, Iwasato T, Itohara S, Erzurumlu RS (2005) Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol 485:280-292.
41. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P, Andersen P (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA 92:9235-9239.
42. Lonart G (2002) RIM1: an edge for presynaptic plasticity. Trends Neurosci 25:329-332.
43. Lonart G, Sudhof TC (1998) Region-specific phosphorylation of rabphilin in mossy fiber nerve terminals of the hippocampus. J Neurosci 18:634-640.
44. Lonart G, Sudhof TC (2001) Characterization of rabphilin phosphorylation using phospho-specific antibodies. Neuropharmacology 41:643-649.
45. Lonart G, Schoch S, Kaeser PS, Larkin CJ, Sudhof TC, Linden DJ (2003) Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 115:49-60.
46. Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci 4:276-289.
47. Lu HC, Gonzalez E, Crair MC (2001) Barrel cortex critical period plasticity is independent of changes inNMDAreceptor subunit composition. Neuron 32:619-634.
48. Lu HC, She WC, Plas DT, Neumann PE, Janz R, Crair MC (2003) Adenylyl cyclase I regulates AMPA receptor trafficking during mouse cortical 'barrel' map development. Nat Neurosci 6:939-947.
49. Manabe T, Nicoll RA (1994) Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265:1888-1892.
50. McLaughlin T, Torborg CL, Feller MB, O'Leary DD (2003) Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40:1147-1160.
51. Murphy GJ, Glickfeld LL, Balsen Z, Isaacson JS (2004) Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals. J Neurosci 24:3023-3030.
52. Nagy G, Reim K, Matti U, Brose N, Binz T, Rettig J, Neher E, Sorensen JB (2004) Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 41:417-429.
53. O'Leary DD, Fawcett JW, CowanWM (1986) Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J Neurosci 6:3692-3705.
54. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2:805-811.
55. Persico AM, Mengual E, Moessner R, Hall FS, Revay RS, Sora I, Arellano J, DeFelipe J, Gimenez-Amaya JM, Conciatori M, Marino R, Baldi A, Cabib S, Pascucci T, Uhl GR, Murphy DL, Lesch KP, Keller F, Hall SF (2001) Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J Neurosci 21:6862-6873.
56. Pinto DJ, Hartings JA, Brumberg JC, Simons DJ (2003) Cortical damping: analysis of thalamocortical response transformations in rodent barrel cortex. Cereb Cortex 13:33-44.
57. Plas DT, Visel A, Gonzalez E, She WC, CrairMC (2004) Adenylate cyclase 1 dependent refinement of retinotopic maps in the mouse. Vision Res 44:3357-3364.
58. Ravary A, Muzerelle A, Herve D, Pascoli V, Ba-Charvet KN, Girault JA, Welker E, Gaspar P (2003) Adenylate cyclase 1 as a key actor in the refinement of retinal projection maps. J Neurosci 23:2228-2238.
59. Rebsam A, Seif I, Gaspar P (2002) Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice. J Neurosci 22:8541-8552.
60. 2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal autapses. J Neurosci 18:2849-2855.
61. Rhoades RW, Bennett-Clarke CA, Shi MY, Mooney RD (1994) Effects of 5-HT on thalamocortical synaptic transmission in the developing rat. J Neurophysiol 72:2438-2450.
62. Risinger C, Bennett MK (1999) Differential phosphorylation of syntaxin and synaptosome-associated protein of 25 kDa (SNAP-25) isoforms. J Neurochem 72:614-624.
63. Rosahl TW, Geppert M, Spillane D, Herz J, Hammer RE, Malenka RC, Sudhof TC (1993) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75:661-670.
64. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
65. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262:754-757.
66. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol (Lond) 531:807-826.
67. Ruthazer ES, Akerman CJ, ClineHT (2003) Control of axon branch dynamics by correlated activity in vivo. Science 301:66-70.
68. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M, De Maeyer E, Murphy DL, Mossner R, Lesch KP, Hen R, Seif I (2001) Excess activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase A and 5-HT transporter knock-out mice. J Neurosci 21:884-896.
69. Schlaggar BL, O'Leary DD (1991) Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science 252:1556-1560.
70. Schluter OM, Schnell E, Verhage M, Tzonopoulos T, Nicoll RA, Janz R, Malenka RC, Geppert M, Sudhof TC (1999) Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J Neurosci 19:5834-5846.
71. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Sudhof TC (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321-326.
72. Senft SL, Woolsey TA (1991) Growth of thalamic afferents into mouse barrel cortex. Cereb Cortex 1:308-335.
73. Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311-330.
74. Sretavan DW, Shatz CJ, Stryker MP (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468-471.
75. 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.
76. Van der Loos H, Dorfl J (1978) Does the skin tell the somatosensory cortex how to construct a map of the periphery? Neurosci Lett 7:23-30.
77. Van der Loos H, Dorfl J, Welker E (1984) Variation in pattern of mystacial vibrissae in mice. A quantitative study of ICR stock and several inbred strains. J Hered 75:326-336.
78. Van der Loos H, Welker E, Dorfl J, Rumo G (1986) Selective breeding for variations in patterns of mystacial vibrissae of mice. Bilaterally symmetrical strains derived from ICR stock. J Hered 77:66-82.
79. Wang Y, Sudhof TC (2003) Genomic definition of RIM proteins: evolutionary amplification of a family of synaptic regulatory proteins. Genomics 81:126-137.
80. Welker E, Armstrong-James M, Bronchti G, Qurednik W, Gheorghita-Baechler F, Dubois R, Guernsey DL, Van der Loos H, Neumann PE (1996) Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless. Science 271:1864-1867.
81. 2+ sensitivity of vesicle pool depletion at a fast CNS synapse. J Neurosci 23:7059-7068.
82. Woolsey TA, Van der LoosH (1970) The structural organization of layer IV in the somatosensory region (SI) of the mouse cerebral cortex. Brain Res 17:205-242.
83. Yanagisawa T, Tsumoto T, Kimura F (2004) Transiently higher release probability during critical period at thalamocortical synapses in the mouse barrel cortex: relevance to differential short-term plasticity of AMPA and NMDA EPSCs and possible involvement of silent synapses. Eur J Neurosci 20:3006-3018.
84. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
85. Zhang LI, Tao HW, Holt CE, Harris WA, Poo M (1998) A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37-44.
86. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.