Dopaminergic axons preferentially innervate dendritic spines with hyperactive glutamatergic synapses in the rat striatum

Brain Research

Volumn 1486, Issue , 2012, Pages 92-102

  Xu, Changlei ^a   Zhao, Junpeng ^a   Liu, Yujun ^a   Zeng, Xianzhi ^b   Jia, Yan ^a   Wang, Ying ^a   Jiang, Xiaohua ^a   Xu, Qunyuan ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b JIAXING UNIVERSITY   (China)

Author keywords

Asymmetric synapse; Dendritic spines; Dopaminergic terminals; Glutamatergic terminals; Medium spiny neurons

Indexed keywords

AMINE; DEXTRAN DERIVATIVE; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITIC SPINE; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; GLUTAMATERGIC SYNAPSE; IMMUNOREACTIVITY; INNERVATION; MALE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPSE; THALAMUS;

ANIMALS; AXONS; CORPUS STRIATUM; DENDRITIC SPINES; DOPAMINERGIC NEURONS; GLUTAMIC ACID; MALE; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

RATTUS;

EID: 84868541795     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.09.032     Document Type: Article

References (50)

1. L.F. Agnati, G. Leo, A. Zanardi, S. Genedani, A. Rivera, K. Fuxe, and D. Guidolin Volume transmission and wiring transmission from cellular to molecular networks: history and perspectives Acta Physiol. 187 2006 329 344
2. E. Bezard, and C.E. Gross Compensatory mechanisms in experimental and human parkinsonism: towards a dynamic approach Prog. Neurobiol. 55 1998 93 116
3. P.A. Buchs, and D. Muller Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses Proc. Natl. Acad. Sci. U.S.A 93 1996 8040 8045
4. M.J. Cabirol-Pol, A. Mizrahi, J. Simmers, and P. Meyrand Combining laser scanning confocal microscopy and electron microscopy to determine sites of synaptic contact between two identified neurons J. Neurosci. Methods 97 2000 175 181
5. I. Caille, B. Dumartin, and B. Bloch Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation Brain Res. 730 1996 17 31
6. P. Calabresi, B. Picconi, A Tozzi, and M. Di Filippo Dopamine-mediated regulation of corticostriatal synaptic plasticity Trends Neurosci. 30 2007 211 219
7. P. Calabresi, A. Pisani, N.B. Mercuri, and G. Bernardi The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia Trends Neurosci. 19 1996 19 24
8. R.K.S. Calverley, and D.G. Jones Contributions of dendritic spines and perforated synapses to synaptic plasticity Brain Res. Rev. 15 1990 215 249
9. B.L. d'Incamps, J. Destombes, D. Thiesson, R. Hellio, X. Lasserre, N. Kouchtir-Devanne, L. Jami, and D. Zytnicki Indications for GABA-immunoreactive axo-axonic contacts on the intraspinal arborization of a lb fiber in cat: a confocal microscope study J. Neurosci. 18 1998 10030 10036
10. M. Day, Z.F. Wang, J. Ding, X.H. An, C.A. Ingham, A.F. Shering, D. Wokosin, E. Ilijic, Z.X. Sun, A.R. Sampson, E. Mugnaini, A.Y. Deutch, S.R. Sesack, G.W. Arbuthnott, and D.J. Surmeier Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models Nat. Neurosci. 9 2006 251 259
11. L. Descarries, K.C. Watkins, S. Garcia, O. Bosler, and G. Doucet Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: a quantitative autoradiographic and immunocytochemical analysis J. Comp. Neurol. 375 1996 167 186
12. G. Di Cristo, C. Wu, B. Chattopadhyaya, F. Ango, G. Knott, E. Welker, K. Svoboda, and Z.J. Huang Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs Nat Neurosci. 7 2004 1184 11846
13. J.C. Fiala, M. Feinberg, V. Popov, and K.M. Harris Synaptogenesis via dendritic filopodia in developing hippocampal area CA1 J. Neurosci. 18 1998 8900 8911
14. W.B. Gan, J. Grutzendler, W.T. Wong, R.O.L. Wong, and J.W. Lichtman Multicolor DiOlistic labeling of the nervous system using lipophilic dye combinations Neuron 27 2000 219 225
15. Y. Geinisman, F. Morrell, and L. Detoledomorrell Remodeling of synaptic architecture during hippocampal kindling Proc. Natl. Acad. Sci. U.S.A 85 1988 3260 3264
16. S.M. Hersch, B.J. Ciliax, C.A. Gutekunst, H.D. Rees, C.J. Heilman, K.K. Yung, J.P. Bolam, E. Ince, H. Yi, and A.I. Levey Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents J. Neurosci. 15 1995 5222 5237
17. S.A. Hires, Y.L. Zhu, and R.Y. Tsien Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters Proc. Natl. Acad. Sci. U.S.A 105 2008 4411 4416
18. C.A. Ingham, S.H. Hood, P. Taggart, and G.W. Arbuthnott Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway J. Neurosci. 18 1998 4732 4743
19. N. Kalisman, G. Silberberg, and H. Markram The neocortical microcircuit as a tabula rasa Proc. Natl. Acad. Sci. U.S.A 102 2005 880 885
20. T. Kaneko, and F. Fujiyama Complementary distribution of vesicular glutamate transporters in the central nervous system Neurosci. Res. 42 2002 243 250
21. A.E. Kincaid, T. Zheng, and C.J. Wilson Connectivity and convergence of single corticostriatal axons J. Neurosci. 18 1998 4722 4731
22. R. Kotter Postsynaptic integration of glutamatergic and dopaminergic signals in the striatum Prog. Neurobiol. 44 1994 163 196
23. Y. Kubota, S. Hatada, S. Kondo, F. Karube, and Y. Kawaguchi Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents J. Neurosci. 27 2007 1139 1150
24. L. Kung, M. Force, D.J. Chute, and R.C. Roberts Immunocytochemical localization of tyrosine hydroxylase in the human striatum: A postmortem ultrastructural study J. Comp. Neurol. 390 1998 52 62
25. C.J. Lacey, J.P. Bolam, and P.J. Magill Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections J. Neurosci. 27 2007 4374 4384
26. M. Matsuzaki, N. Honkura, G.C.R. Ellis-Davies, and H. Kasai Structural basis of long-term potentiation in single dendritic spines Nature 429 2004 761 766
27. F. Mora, G. Segovia, and A. del Arco Glutamate-dopamine-GABA interactions in the aging basal ganglia Brain Res. Rev. 58 2008 340 353
28. J. Moss, and J.P. Bolam A dopaminergic axon lattice in the striatum and its relationship with cortical and thalamic terminals J. Neurosci. 28 2008 11221 11230
29. M.D. Neely, D.E. Schmidt, and A.Y. Deutch Cortical regulation of dopamine depletion-induced dendritic spine loss in striatal medium spiny neurons Neuroscience 149 2007 457 464
30. M.A. Nieto Molecular biology of axon guidance Neuron 17 1996 1039 1048
31. K.I. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity Nat. Neurosci. 7 2004 1104 1112
32. M.J. Olave, and D.J. Maxwell Neurokinin-1 projection cells in the rat dorsal horn receive synaptic contacts from axons that possess alpha(2C)-adrenergic receptors J. Neurosci. 23 2003 6837 6846
33. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Co-ordinates 2005 Elsevier Academic Press San Diego
34. A. Peters, S.L. Palay, and H. deF. Webster The Fine Structure of The Nervous System 1991 Oxford University Press New York
35. M.A. Raghanti, C.D. Stimpson, J.L. Marcinkiewicz, J.M. Erwin, P.R. Hof, and C.C. Sherwood Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: a comparative study Neuroscience 155 2008 203 220
36. D.V. Raju, D.J. Shah, T.M. Wright, R.A. Hall, and Y. Smith Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats J. Comp. Neurol. 499 2006 231 243
37. Y. Schmitz, J Luccarelli, M. Kim, M. Wang, and D. Sulzer Glutamate controls growth rate and branching of dopaminergic axons J. Neurosci. 29 2009 11973 11981
38. L. Scott, M.S. Kruse, H. Forssberg, H. Brismar, P. Greengard, and A. Aperia Selective up-regulation of dopamine D1 receptors in dendritic spines by NMDA receptor activation Proc. Natl. Acad. Sci. U.S.A 99 2002 1661 1664
39. L. Scott, S. Zelenin, S. Malmersjo, J.M. Kowalewski, E. Zettergren-Markus, A.C. Nairn, P. Greengard, H. Brismar, and A. Aperia Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines Eur. Neuropsychopharmacol. 16 2006 S170
40. S.R. Sesack, D.B. Carr, N. Omelchenko, and A. Pinto Anatomical Substrates For Glutamate-Dopamine Interactions: Evidence For Specificity of Connections And Extrasynaptic Actions 2003 New York Acad Sciences New York
41. A.D. Smith, and J.P. Bolam The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons Trends Neurosci. 13 1990 259 265
42. A. Stepanyants, and D.B. Chklovskii Neurogeometry and potential synaptic connectivity Trends Neurosci. 28 2005 387 394
43. A. Stepanyants, P.R. Hof, and D.B. Chklovskii Geometry and structural plasticity of synaptic connectivity Neuron 34 2002 275 288
44. A. Stepanyants, G. Tamas, and D.B. Chklovskii Class-specific features of neuronal wiring Neuron 43 2004 251 259
45. M. TessierLavigne, and C.S. Goodman The molecular biology of axon guidance Science 274 1996 1123 1133
46. N. Toni, E.M. Teng, E.A. Bushong, J.B. Aimone, C.M. Zhao, A. Consiglio, H. van Praag, M.E. Martone, M.H. Ellisman, and F.H. Gage Synapse formation on neurons born in the adult hippocampus Nat. Neurosci. 10 2007 727 734
47. J.R. Wickens, J.N.J. Reynolds, and B.I. Hyland Neural mechanisms of reward-related motor learning Curr. Opin. Neurobiol. 13 2003 685 690
48. C.J. Wilson, P.M. Groves, S.T. Kitai, and J.C. Linder 3-Dimensional structure of dendritic spines in the rat neostriatum J. Neurosci. 3 1983 383 398
49. H. Zhang, and D. Sulzer Glutamate spillover in the striatum depresses dopaminergic transmission by activating group I metabotropic glutamate receptors J. Neurosci. 23 2003 10585 10592
50. Q. Zhou, K.J. Homma, and M.M. Poo Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses Neuron 44 2004 749 757