Identifying roles for neurotransmission in circuit assembly: Insights gained from multiple model systems and experimental approaches

BioEssays

Volumn 33, Issue 1, 2011, Pages 61-72

  Bleckert, Adam ^a   Wong, Rachel O L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Circuit refinement; Neuronal connectivity; Synapse elimination; Synapse formation; Synaptic transmission

Indexed keywords

INFORMATION PROCESSING; MODEL; NERVE CELL NETWORK; NERVE CONDUCTION; NERVOUS SYSTEM; NEUROTRANSMISSION; NONHUMAN; REVIEW; TECHNIQUE;

ADULT; BIOLOGICAL ASSAY; GENE REGULATORY NETWORKS; HUMANS; MODELS, BIOLOGICAL; NERVOUS SYSTEM; NEURONS; PHOTORECEPTOR CELLS, VERTEBRATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 78650010651     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000095     Document Type: Review

References (101)

1. Hubel DH, Wiesel TN, LeVay S. 1977. Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278: 377-409.
2. LeVay S, Wiesel TN, Hubel DH. 1980. The development of ocular dominance columns in normal and visually deprived monkeys. J Comp Neurol 191: 1-51.
3. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389-442.
4. Hume RI, Role LW, Fischbach GD. 1983. Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes. Nature 305: 632-4.
5. Taylor J, Docherty M, Gordon-Weeks PR. 1990. GABAergic growth cones: release of endogenous gamma-aminobutyric acid precedes the expression of synaptic vesicle antigens. J Neurochem 54: 1689-99.
6. Ziv NE, Smith SJ. 1996. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17: 91-102.
7. Smith SJ, Jahr CE. 1992. Rapid induction of filopodial sprouting by application of glutamate to hippocampal neurons. In Letourneau PC, Kater SB, Macagno ER. ed; The Nerve Growth Cone. New York: Raven Press. p 19-26.
8. Wong WT, Wong RO. 2001. Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nat Neurosci 4: 351-2.
9. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, et al. 2002. Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36: 635-48.
10. Rao A, Craig AM. 1997. Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19: 801-12.
11. Varoqueaux F, Sigler A, Rhee JS, Brose N, et al. 2002. Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci USA 99: 9037-42.
12. Verhage M, Maia AS, Plomp JJ, Brussaard AB, et al. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287: 864.
13. Okabe S, Kim HD, Miwa A, Kuriu T, et al. 1999. Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 2: 804-11.
14. Wu G, Malinow R, Cline HT. 1996. Maturation of a central glutamatergic synapse. Science 274: 972-6.
15. Redfern PA. 1970. Neuromuscular transmission in new-born rats. J Physiol 209: 701-709.
16. Walsh MK, Lichtman JW. 2003. In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37: 67-73.
17. Huberman AD, Feller MB, Chapman B. 2008. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31: 479-509.
18. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274: 1133-8.
19. Leamey CA, Van Wart A, Sur M. 2009. Intrinsic patterning and experience-dependent mechanisms that generate eye-specific projections and binocular circuits in the visual pathway. Curr Opin Neurobiol 19: 181-7.
20. Chen C, Regehr WG. 2000. Developmental remodeling of the retinogeniculate synapse. Neuron 28: 955-66.
21. Hooks BM, Chen C. 2006. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52: 281-91.
22. Mariani J, Changeux JP. 1981. Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J Neurosci 1: 696-702.
23. Hashimoto K, Ichikawa R, Takechi H, Inoue Y, et al. 2001. Roles of glutamate receptor delta 2 subunit (GluRdelta 2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development. J Neurosci 21: 9701-12.
24. Lorenzetto E, Caselli L, Feng G, Yuan W, et al. 2009. Genetic perturbation of postsynaptic activity regulates synapse elimination in developing cerebellum. Proc Natl Acad Sci USA 106: 16475-80.
25. Miyazaki T, Hashimoto K, Shin HS, Kano M, et al. 2004. P/Q-type Ca2+ channel alpha1A regulates synaptic competition on developing cerebellar Purkinje cells. J Neurosci 24: 1734-43.
26. Sugihara I, Wu HS, Shinoda Y. 2001. The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to Cerebellar compartmentalization. J Neurosci 21: 7715-23.
27. Sugihara I. 2006. Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5: 15-22.
28. Buffelli M, Burgess RW, Feng G, Lobe CG, et al. 2003. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424: 430-4.
29. Bosman LW, Takechi H, Hartmann J, Eilers J, et al. 2008. Homosynaptic long-term synaptic potentiation of the "winner" climbing fiber synapse in developing Purkinje cells. J Neurosci 28: 798-807.
30. Hata Y, Stryker MP. 1994. Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. Science 265: 1732-5.
31. Kasthuri N, Lichtman JW. 2003. The role of neuronal identity in synaptic competition. Nature 424: 426-30.
32. Bi G, Poo M. 2001. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24: 139-66.
33. Silver MA, Stryker MP. 1999. Synaptic density in geniculocortical afferents remains constant after monocular deprivation in the cat. J Neurosci 19: 10829-42.
34. Hashimoto K, Kano M. 2003. Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38: 785-96.
35. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, et al. 2009. Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63: 106-18.
36. Lohmann C, Bonhoeffer T. 2008. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 59: 253-60.
37. Threadgill R, Bobb K, Ghosh A. 1997. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19: 625-34.
38. Zou DJ, Cline HT. 1999. Postsynaptic calcium/calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J Neurosci 19: 8909-18.
39. Cohen-Cory S. 1999. BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo. J Neurosci 19: 9996-10003.
40. Hooks BM, Chen C. 2008. Vision triggers an experience-dependent sensitive period at the retinogeniculate synapse. J Neurosci 28: 4807-17.
41. Blankenship AG, Feller MB. 2010. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29.
42. Johns DC, Marx R, Mains RE, O'Rourke B, et al. 1999. Inducible genetic suppression of neuronal excitability. J Neurosci 19: 1691-7.
43. Schiavo G, Benfenati F, Poulain B, Rossetto O, et al. 1992. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359: 832-5.
44. Altar CA, DiStefano PS. 1998. Neurotrophin trafficking by anterograde transport. Trends Neurosci 21: 433-7.
45. Balice-Gordon RJ, Lichtman JW. 1994. Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372: 519-24.
46. Rajan I, Witte S, Cline HT. 1999. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J Neurobiol 38: 357-68.
47. Sin WC, Haas K, Ruthazer ES, Cline HT. 2002. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419: 475-80.
48. Ewald RC, Van Keuren-Jensen KR, Aizenman CD, Cline HT. 2008. Roles of NR2A and NR2B in the development of dendritic arbor morphology in vivo. J Neurosci 28: 850-61.
49. 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: 477-92.
50. Lee LJ, Lo FS, Erzurumlu RS. 2005. NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci 25: 2304-11.
51. Espinosa JS, Wheeler DG, Tsien RW, Luo L. 2009. Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B. Neuron 62: 205-17.
52. Mizuno H, Hirano T, Tagawa Y. 2010. Pre-synaptic and post-synaptic neuronal activity supports the axon development of callosal projection neurons during different post-natal periods in the mouse cerebral cortex. Eur J Neurosci 31: 410-24.
53. Yamada A, Uesaka N, Hayano Y, Tabata T, et al. 2010. Role of pre- and postsynaptic activity in thalamocortical axon branching. Proc Natl Acad Sci USA 107: 7562-7.
54. Tao HW, Poo M. 2001. Retrograde signaling at central synapses. Proc Natl Acad Sci USA 98: 11009-15.
55. Lom B, Cogen J, Sanchez AL, Vu T, et al. 2002. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo. J Neurosci 22: 7639-49.
56. Du JL, Wei HP, Wang ZR, Wong ST, et al. 2009. Long-range retrograde spread of LTP and LTD from optic tectum to retina. Proc Natl Acad Sci USA 106: 18890-6.
57. Zou DJ, Chesler A, Firestein S. 2009. How the olfactory bulb got its glomeruli: a just so story? Nat Rev Neurosci 10: 611-8.
58. Belluscio L, Gold GH, Nemes A, Axel R. 1998. Mice deficient in G(olf) are anosmic. Neuron 20: 69-81.
59. Lin DM, Wang F, Lowe G, Gold GH, et al. 2000. Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26: 69-80.
60. Zou DJ, Feinstein P, Rivers AL, Mathews GA, et al. 2004. Postnatal refinement of peripheral olfactory projections. Science 304: 1976-9.
61. Kerr MA, Belluscio L. 2006. Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nat Neurosci 9: 484-6.
62. Yu CR, Power J, Barnea G, O'Donnell S, et al. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42: 553-66.
63. Tripodi M, Evers JF, Mauss A, Bate M, et al. 2008. Structural homeostasis: compensatory adjustments of dendritic arbor geometry in response to variations of synaptic input. PLoS Biol 6: e260.
64. Kerschensteiner D, Morgan JL, Parker ED, Lewis RM, et al. 2009. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 460: 1016-20.
65. Bodnarenko SR, Chalupa LM. 1993. Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364: 144-6.
66. Tagawa Y, Sawai H, Ueda Y, Tauchi M, et al. 1999. Immunohistological studies of metabotropic glutamate receptor subtype 6-deficient mice show no abnormality of retinal cell organization and ganglion cell maturation. J Neurosci 19: 2568-79.
67. Harms KJ, Craig AM. 2005. Synapse composition and organization following chronic activity blockade in cultured hippocampal neurons. J Comp Neurol 490: 72-84.
68. Riccio RV, Matthews MA. 1985. Effects of intraocular tetrodotoxin on dendritic spines in the developing rat visual cortex: a Golgi analysis. Brain Res 351: 173-82.
69. Ultanir SK, Kim JE, Hall BJ, Deerinck T, et al. 2007. Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Natl Acad Sci USA 104: 19553-8.
70. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66: 15-36.
71. Kim IJ, Zhang Y, Meister M, Sanes JR. 2010. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci 30: 1452-62.
72. Mumm JS, Williams PR, Godinho L, Koerber A, et al. 2006. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52: 609-21.
73. Jennings C. 1994. Developmental neurobiology. Death of a synapse. Nature 372: 498.
74. Cramer KS, Karam SD, Bothwell M, Cerretti DP, et al. 2002. Expression of EphB receptors and EphrinB ligands in the developing chick auditory brainstem. J Comp Neurol 452: 51-64.
75. Cramer KS, Bermingham-McDonogh O, Krull CE, Rubel EW. 2004. EphA4 signaling promotes axon segregation in the developing auditory system. Dev Biol 269: 26-35.
76. Tao HW, Zhang LI, Engert F, Poo M. 2001. Emergence of input specificity of ltp during development of retinotectal connections in vivo. Neuron 31: 569-80.
77. Wässle H, Puller C, Müller F, Haverkamp S. 2009. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29: 106-17.
78. Reese BE. 2010. Development of the retina and optic pathway. Vision Res, in press, DOI: 10.1016/j.visres.2010.07.010.
79. Reh TA, Constantine-Paton M. 1985. Eye-specific segregation requires neural activity in three-eyed Rana pipiens. J Neurosci 5: 1132-43.
80. Lichtman JW, Livet J, Sanes JR. 2008. A technicolour approach to the connectome. Nat Rev Neurosci 9: 417-22.
81. Huberman AD. 2007. Mechanisms of eye-specific visual circuit development. Curr Opin Neurobiol 17: 73-80.
82. Dan Y, Poo MM. 2004. Spike timing-dependent plasticity of neural circuits. Neuron 44: 23-30.
83. Lin AC, Holt CE. 2008. Function and regulation of local axonal translation. Curr Opin Neurobiol 18: 60-8.
84. Sutton MA, Schuman EM. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127: 49-58.
85. Chen Y, Ghosh A. 2005. Regulation of dendritic development by neuronal activity. J Neurobiol 64: 4-10.
86. Jan YN, Jan LY. 2010. Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11: 316-28.
87. Tao HW, Poo MM. 2005. Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45: 829-36.
88. Engert F, Tao HW, Zhang LI, Poo MM. 2002. Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419: 470-5.
89. Li Y, Van Hooser SD, Mazurek M, White LE, et al. 2008. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456: 952-6.
90. White LE, Fitzpatrick D. 2007. Vision and cortical map development. Neuron 56: 327-38.
91. Sørensen JB, Matti U, Wei SH, Nehring RB, et al. 2002. The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc Natl Acad Sci USA 99: 1627-32.
92. Haas K, Li J, Cline HT. 2006. AMPA receptors regulate experience-dependent dendritic arbor growth in vivo. Proc Natl Acad Sci USA 103: 12127-31.
93. Hua JY, Smear MC, Baier H, Smith SJ. 2005. Regulation of axon growth in vivo by activity-based competition. Nature 434: 1022-6.
94. Stuermer CA, Rohrer B, Münz H. 1990. Development of the retinotectal projection in zebrafish embryos under TTX-induced neural-impulse blockade. J Neurosci 10: 3615-26.
95. Gnuegge L, Schmid S, Neuhauss SC. 2001. Analysis of the activity-deprived zebrafish mutant macho reveals an essential requirement of neuronal activity for the development of a fine-grained visuotopic map. J Neurosci 21: 3542-8.
96. Ben Fredj N, Hammond S, Otsuna H, Chien CB, et al. 2010. Synaptic activity and activity-dependent competition regulates axon arbor maturation, growth arrest, and territory in the retinotectal projection. J Neurosci 30: 10939-51.
97. Burrone J, O'Byrne M, Murthy VN. 2002. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420: 414-8.
98. Murthy VN, Schikorski T, Stevens CF, Zhu Y. 2001. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32: 673-82.
99. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, et al. 1998. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391: 892-6.
100. Hashimoto K, Yoshida T, Sakimura K, Mishina M, et al. 2009. Influence of parallel fiber-Purkinje cell synapse formation on postnatal development of climbing fiber-Purkinje cell synapses in the cerebellum. Neuroscience 162: 601-11.
101. Deitch JS, Rubel EW. 1984. Afferent influences on brain stem auditory nuclei of the chicken: time course and specificity of dendritic atrophy following deafferentation. J Comp Neurol 229: 66-79.