Refinement of the Retinogeniculate Synapse by Bouton Clustering

Neuron

Volumn 84, Issue 2, 2014, Pages 332-339

  Hong, Y Kate ^a,b   Park, SuHong ^a   Litvina, Elizabeth Y ^a   Morales, Jose ^a   Sanes, Joshua R ^b   Chen, Chinfei ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BOUTON CLUSTERING; BRAIN SYNAPTOSOME; CONTROLLED STUDY; LATERAL GENICULATE BODY; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PRESYNAPTIC MEMBRANE; RETINA GANGLION CELL; RETINOGENICULATE SYNAPSE; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL FIELD; ANIMAL; GENICULATE BODY; NERVE CELL; NERVE FIBER; PHYSIOLOGY; RETINA; SYNAPTOSOME; TRANSGENIC MOUSE; VISUAL SYSTEM;

ANIMALS; AXONS; GENICULATE BODIES; MICE; MICE, TRANSGENIC; NEURONS; PRESYNAPTIC TERMINALS; RETINA; RETINAL GANGLION CELLS; SYNAPSES; VISUAL PATHWAYS;

EID: 84908248912     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.08.059     Document Type: Article

References (57)

1. Antonini A., Stryker M.P. Rapid remodeling of axonal arbors in the visual cortex. Science 1993, 260:1819-1821.
2. Antonini A., Fagiolini M., Stryker M.P. Anatomical correlates of functional plasticity in mouse visual cortex. J.Neurosci. 1999, 19:4388-4406.
3. Binzegger T., Douglas R.J., Martin K.A.C. Stereotypical bouton clustering of individual neurons in cat primary visual cortex. J.Neurosci. 2007, 27:12242-12254.
4. Buffelli M., Burgess R.W., Feng G., Lobe C.G., Lichtman J.W., Sanes J.R. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 2003, 424:430-434.
5. Chen C., Regehr W.G. Developmental remodeling of the retinogeniculate synapse. Neuron 2000, 28:955-966.
6. Cheng T.-W., Liu X.-B., Faulkner R.L., Stephan A.H., Barres B.A., Huberman A.D., Cheng H.-J. Emergence of lamina-specific retinal ganglion cell connectivity by axon arbor retraction and synapse elimination. J.Neurosci. 2010, 30:16376-16382.
7. Cleland B.G., Dubin M.W., Levick W.R. Simultaneous recording of input and output of lateral geniculate neurones. Nat. New Biol. 1971, 231:191-192.
8. Coleman J.E., Nahmani M., Gavornik J.P., Haslinger R., Heynen A.J., Erisir A., Bear M.F. Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. J.Neurosci. 2010, 30:9670-9682.
9. Cruz-Martín A., El-Danaf R.N., Osakada F., Sriram B., Dhande O.S., Nguyen P.L., Callaway E.M., Ghosh A., Huberman A.D. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 2014, 507:358-361.
10. De Paola V., Holtmaat A., Knott G., Song S., Wilbrecht L., Caroni P., Svoboda K. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 2006, 49:861-875.
11. Dhande O.S., Hua E.W., Guh E., Yeh J., Bhatt S., Zhang Y., Ruthazer E.S., Feller M.B., Crair M.C. Development of single retinofugal axon arbors in normal and β2 knock-out mice. J.Neurosci. 2011, 31:3384-3399.
12. Erzurumlu R.S., Jhaveri S., Schneider G.E. Distribution of morphologically different retinal axon terminals in the hamster dorsal lateral geniculate nucleus. Brain Res. 1988, 461:175-181.
13. Famiglietti E.V., Peters A. The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J.Comp. Neurol. 1972, 144:285-334.
14. Hamos J.E., Van Horn S.C., Raczkowski D., Sherman S.M. Synaptic circuits involving an individual retinogeniculate axon in the cat. J.Comp. Neurol. 1987, 259:165-192.
15. Hashimoto K., Ichikawa R., Kitamura K., Watanabe M., Kano M. Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 2009, 63:106-118.
16. Hong Y.K., Chen C. Wiring and rewiring of the retinogeniculate synapse. Curr. Opin. Neurobiol. 2011, 21:228-237.
17. Hooks B.M., Chen C. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 2006, 52:281-291.
18. Hooks B.M., Chen C. Vision triggers an experience-dependent sensitive period at the retinogeniculate synapse. J.Neurosci. 2008, 28:4807-4817.
19. Hua J.Y., Smear M.C., Baier H., Smith S.J. Regulation of axon growth invivo by activity-based competition. Nature 2005, 434:1022-1026.
20. Huberman A.D. Mechanisms of eye-specific visual circuit development. Curr. Opin. Neurobiol. 2007, 17:73-80.
21. Huberman A.D., Manu M., Koch S.M., Susman M.W., Lutz A.B., Ullian E.M., Baccus S.A., Barres B.A. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 2008, 59:425-438.
22. Jaubert-Miazza L., Green E., Lo F.-S., Bui K., Mills J., Guido W. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis. Neurosci. 2005, 22:661-676.
23. Kay J.N., De La Huerta I., Kim I.-J., Zhang Y., Yamagata M., Chu M.W., Meister M., Sanes J.R. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J.Neurosci. 2011, 31:7753-7762.
24. Keller-Peck C.R., Walsh M.K., Gan W.B., Feng G., Sanes J.R., Lichtman J.W. Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 2001, 31:381-394.
25. Kim I.-J., Zhang Y., Yamagata M., Meister M., Sanes J.R. Molecular identification of a retinal cell type that responds to upward motion. Nature 2008, 452:478-482.
26. Kim I.-J., Zhang Y., Meister M., Sanes J.R. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J.Neurosci. 2010, 30:1452-1462.
27. Kleindienst T., Winnubst J., Roth-Alpermann C., Bonhoeffer T., Lohmann C. Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron 2011, 72:1012-1024.
28. Knudsen E.I., Zheng W., DeBello W.M. Traces of learning in the auditory localization pathway. Proc. Natl. Acad. Sci. USA 2000, 97:11815-11820.
29. Koch S.M., Ullian E.M. Neuronal pentraxins mediate silent synapse conversion in the developing visual system. J.Neurosci. 2010, 30:5404-5414.
30. Krahe T.E., El-Danaf R.N., Dilger E.K., Henderson S.C., Guido W. Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. J.Neurosci. 2011, 31:17437-17448.
31. Land P.W., Kyonka E., Shamalla-Hannah L. Vesicular glutamate transporters in the lateral geniculate nucleus: expression of VGLUT2 by retinal terminals. Brain Res. 2004, 996:251-254.
32. Li J., Erisir A., Cline H. Invivo time-lapse imaging and serial section electron microscopy reveal developmental synaptic rearrangements. Neuron 2011, 69:273-286.
33. Ling C., Schneider G.E., Jhaveri S. Target-specific morphology of retinal axon arbors in the adult hamster. Vis. Neurosci. 1998, 15:559-579.
34. Linkenhoker B.A., von der Ohe C.G., Knudsen E.I. Anatomical traces of juvenile learning in the auditory system of adult barn owls. Nat. Neurosci. 2005, 8:93-98.
35. Mason C.A. Development of terminal arbors of retino-geniculate axons in the kitten-I. Light microscopical observations. Neuroscience 1982, 7:541-559.
36. Mastronarde D.N. Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: receptive-field properties and retinal inputs. Vis. Neurosci. 1992, 8:407-441.
37. McBride T.J., Rodriguez-Contreras A., Trinh A., Bailey R., Debello W.M. Learning drives differential clustering of axodendritic contacts in the barn owl auditory system. J.Neurosci. 2008, 28:6960-6973.
38. McLaughlin T., Torborg C.L., Feller M.B., O'Leary D.D. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 2003, 40:1147-1160.
39. Meyer M.P., Smith S.J. Evidence from invivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J.Neurosci. 2006, 26:3604-3614.
40. Morgan J.L., Soto F., Wong R.O.L., Kerschensteiner D. Development of cell type-specific connectivity patterns of converging excitatory axons in the retina. Neuron 2011, 71:1014-1021.
41. Portera-Cailliau C., Weimer R.M., De Paola V., Caroni P., Svoboda K. Diverse modes of axon elaboration in the developing neocortex. PLoS Biol. 2005, 3:e272.
42. Purves D., Lichtman J.W. Elimination of synapses in the developing nervous system. Science 1980, 210:153-157.
43. Ruthazer E.S., Li J., Cline H.T. Stabilization of axon branch dynamics by synaptic maturation. J.Neurosci. 2006, 26:3594-3603.
44. Silver M.A., Stryker M.P. Synaptic density in geniculocortical afferents remains constant after monocular deprivation in the cat. J.Neurosci. 1999, 19:10829-10842.
45. Snider C.J., Dehay C., Berland M., Kennedy H., Chalupa L.M. Prenatal development of retinogeniculate axons in the macaque monkey during segregation of binocular inputs. J.Neurosci. 1999, 19:220-228.
46. Sretavan D., Shatz C.J. Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 1984, 308:845-848.
47. Stettler D.D., Yamahachi H., Li W., Denk W., Gilbert C.D. Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 2006, 49:877-887.
48. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
49. Sugihara I. Microzonal projection and climbing fiber remodeling in single olivocerebellar axons of newborn rats at postnatal days 4-7. J.Comp. Neurol. 2005, 487:93-106.
50. Sur M., Sherman S.M. Retinogeniculate terminations in cats: morphological differences between X and Y cell axons. Science 1982, 218:389.
51. Sur M., Weller R.E., Sherman S.M. Development of X- and Y-cell retinogeniculate terminations in kittens. Nature 1984, 310:246-249.
52. Takeuchi Y., Asano H., Katayama Y., Muragaki Y., Imoto K., Miyata M. Large-scale somatotopic refinement via functional synapse elimination in the sensory thalamus of developing mice. J.Neurosci. 2014, 34:1258-1270.
53. Tapia J.C., Wylie J.D., Kasthuri N., Hayworth K.J., Schalek R., Berger D.R., Guatimosim C., Seung H.S., Lichtman J.W. Pervasive synaptic branch removal in the mammalian neuromuscular system at birth. Neuron 2012, 74:816-829.
54. Wierenga C.J., Becker N., Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 2008, 11:1044-1052.
55. Winnubst J., Lohmann C. Synaptic clustering during development and learning: the why, when, and how. Front Mol Neurosci 2012, 5:70.
56. Yeow M.B., Peterson E.H. Active zone organization and vesicle content scale with bouton size at a vertebrate central synapse. J.Comp. Neurol. 1991, 307:475-486.
57. Zheng W., Knudsen E.I. Gabaergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J.Neurosci. 2001, 21:4356-4365.