Visual circuit development requires patterned activity mediated by retinal acetylcholine receptors

Neuron

Volumn 84, Issue 5, 2014, Pages 1049-1064

  Burbridge, Timothy J ^a   Xu, Hong Ping ^a   Ackman, James B ^a   Ge, Xinxin ^a   Zhang, Yueyi ^a   Ye, Mei Jun ^a   Zhou, Z Jimmy ^a   Xu, Jian ^b   Contractor, Anis ^b   Crair, Michael C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; NICOTINIC RECEPTOR BETA2; CALCIUM; CYCLIC AMP; CYCLIC GMP; EYE PROTEIN; HOMEODOMAIN PROTEIN; MECLOFENAMIC ACID; MESSENGER RNA; NICOTINIC RECEPTOR; PAIRED BOX TRANSCRIPTION FACTOR; PROSTAGLANDIN SYNTHASE INHIBITOR; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR PAX6;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; IN VIVO STUDY; MOUSE; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE FUNCTION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; RETINA; RETINA GANGLION CELL; VISUAL NERVOUS SYSTEM; ACTION POTENTIAL; AGE; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMISPHERIC DOMINANCE; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; VALIDATION STUDY; VISUAL SYSTEM;

ACTION POTENTIALS; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CYCLIC AMP; CYCLIC GMP; CYCLOOXYGENASE INHIBITORS; EYE PROTEINS; FUNCTIONAL LATERALITY; HOMEODOMAIN PROTEINS; IN VITRO TECHNIQUES; MECLOFENAMIC ACID; MICE; MICE, TRANSGENIC; PAIRED BOX TRANSCRIPTION FACTORS; RECEPTORS, NICOTINIC; REPRESSOR PROTEINS; RETINA; RETINAL GANGLION CELLS; RNA, MESSENGER; VISUAL PATHWAYS;

EID: 84919424542     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.10.051     Document Type: Article

References (63)

1. Ackman J.B., Crair M.C. Role of emergent neural activity in visual map development. Curr. Opin. Neurobiol. 2014, 24:166-175.
2. Ackman J.B., Burbridge T.J., Crair M.C. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 2012, 490:219-225.
3. Bansal A., Singer J.H., Hwang B.J., Xu W., Beaudet A., Feller M.B. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J.Neurosci. 2000, 20:7672-7681.
4. Blankenship A.G., Hamby A.M., Firl A., Vyas S., Maxeiner S., Willecke K., Feller M.B. The role of neuronal connexins 36 and 45 in shaping spontaneous firing patterns in the developing retina. J.Neurosci. 2011, 31:9998-10008.
5. Bunt S.M., Lund R.D. Development of a transient retino-retinal pathway in hooded and albino rats. Brain Res. 1981, 211:399-404.
6. Butts D.A., Kanold P.O., Shatz C.J. A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol. 2007, 5:e61.
7. Cang J., Feldheim D.A. Developmental mechanisms of topographic map formation and alignment. Annu. Rev. Neurosci. 2013, 36:51-77.
8. Cang J., Rentería R.C., Kaneko M., Liu X., Copenhagen D.R., Stryker M.P. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 2005, 48:797-809.
9. Chalupa L.M. Retinal waves are unlikely to instruct the formation of eye-specific retinogeniculate projections. Neural Dev. 2009, 4:25.
10. Chandrasekaran A.R., Plas D.T., Gonzalez E., Crair M.C. Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J.Neurosci. 2005, 25:6929-6938.
11. Crair M.C., Gillespie D.C., Stryker M.P. The role of visual experience in the development of columns in cat visual cortex. Science 1998, 279:566-570.
12. Crair M.C., Horton J.C., Antonini A., Stryker M.P. Emergence of ocular dominance columns in cat visual cortex by 2weeks of age. J.Comp. Neurol. 2001, 430:235-249.
13. Crowley J.C., Katz L.C. Development of ocular dominance columns in the absence of retinal input. Nat. Neurosci. 1999, 2:1125-1130.
14. Crowley J.C., Katz L.C. Early development of ocular dominance columns. Science 2000, 290:1321-1324.
15. 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.
16. Dhande O.S., Bhatt S., Anishchenko A., Elstrott J., Iwasato T., Swindell E.C., Xu H.P., Jamrich M., Itohara S., Feller M.B., Crair M.C. Role of adenylate cyclase 1 in retinofugal map development. J.Comp. Neurol. 2012, 520:1562-1583.
17. Ebert D.H., Greenberg M.E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 2013, 493:327-337.
18. Espinosa J.S., Stryker M.P. Development and plasticity of the primary visual cortex. Neuron 2012, 75:230-249.
19. Feller M.B. Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections. Neural Dev. 2009, 4:24.
20. Feller M.B., Wellis D.P., Stellwagen D., Werblin F.S., Shatz C.J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 1996, 272:1182-1187.
21. Frisén J., Yates P.A., McLaughlin T., Friedman G.C., O'Leary D.D., Barbacid M. Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system. Neuron 1998, 20:235-243.
22. Galli L., Maffei L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 1988, 242:90-91.
23. Godfrey K.B., Eglen S.J., Swindale N.V. A multi-component model of the developing retinocollicular pathway incorporating axonal and synaptic growth. PLoS Comput. Biol. 2009, 5:e1000600.
24. Grubb M.S., Thompson I.D. Visual response properties in the dorsal lateral geniculate nucleus of mice lacking the β2 subunit of the nicotinic acetylcholine receptor. J.Neurosci. 2004, 24:8459-8469.
25. Horton J.C., Hocking D.R. An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J.Neurosci. 1996, 16:1791-1807.
26. Hubel D.H., Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J.Physiol. 1970, 206:419-436.
27. Huberman A.D., Wang G.Y., Liets L.C., Collins O.A., Chapman B., Chalupa L.M. Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science 2003, 300:994-998.
28. Huberman A.D., Feller M.B., Chapman B. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 2008, 31:479-509.
29. Kirkby L.A., Feller M.B. Intrinsically photosensitive ganglion cells contribute to plasticity in retinal wave circuits. Proc. Natl. Acad. Sci. USA 2013, 110:12090-12095.
30. Kirkby L.A., Sack G.S., Firl A., Feller M.B. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron 2013, 80:1129-1144.
31. Lozada A.F., Wang X., Gounko N.V., Massey K.A., Duan J., Liu Z., Berg D.K. Induction of dendritic spines by β2-containing nicotinic receptors. J.Neurosci. 2012, 32:8391-8400.
32. Marquardt T., Ashery-Padan R., Andrejewski N., Scardigli R., Guillemot F., Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 2001, 105:43-55.
33. 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.
34. Meister M., Wong R.O., Baylor D.A., Shatz C.J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 1991, 252:939-943.
35. Mrsic-Flogel T.D., Hofer S.B., Creutzfeldt C., Cloëz-Tayarani I., Changeux J.P., Bonhoeffer T., Hübener M. Altered map of visual space inthe superior colliculus of mice lacking early retinal waves. J.Neurosci. 2005, 25:6921-6928.
36. Nicol X., Voyatzis S., Muzerelle A., Narboux-Nême N., Südhof T.C., Miles R., Gaspar P. cAMP oscillations and retinal activity are permissive for ephrin signaling during the establishment of the retinotopic map. Nat. Neurosci. 2007, 10:340-347.
37. O'Leary D.D., Crespo D., Fawcett J.W., Cowan W.M. The effect of intraocular tetrodotoxin on the postnatal reduction in the numbers of optic nerve axons in the rat. Brain Res. 1986, 395:96-103.
38. O'Leary D.D., Fawcett J.W., Cowan W.M. Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J.Neurosci. 1986, 6:3692-3705.
39. Penn A.A., Riquelme P.A., Feller M.B., Shatz C.J. Competition inretinogeniculate patterning driven by spontaneous activity. Science 1998, 279:2108-2112.
40. Pfeiffenberger C., Yamada J., Feldheim D.A. Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. J.Neurosci. 2006, 26:12873-12884.
41. Rakic P. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 1976, 261:467-471.
42. Rossi F.M., Pizzorusso T., Porciatti V., Marubio L.M., Maffei L., Changeux J.P. Requirement of the nicotinic acetylcholine receptor β 2 subunit for the anatomical and functional development of the visual system. Proc. Natl. Acad. Sci. USA 2001, 98:6453-6458.
43. Ruthazer E.S., Stryker M.P. The role of activity in the development of long-range horizontal connections in area 17 of the ferret. J.Neurosci. 1996, 16:7253-7269.
44. Sanes J.R., Zipursky S.L. Design principles of insect and vertebrate visual systems. Neuron 2010, 66:15-36.
45. Shah R.D., Crair M.C. Retinocollicular synapse maturation and plasticity are regulated by correlated retinal waves. J.Neurosci. 2008, 28:292-303.
46. Shatz C.J., Stryker M.P. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 1988, 242:87-89.
47. Sperry R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 1963, 50:703-710.
48. Stacy R.C., Demas J., Burgess R.W., Sanes J.R., Wong R.O. Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J.Neurosci. 2005, 25:9347-9357.
49. Stafford B.K., Sher A., Litke A.M., Feldheim D.A. Spatial-temporal patterns of retinal waves underlying activity-dependent refinement of retinofugal projections. Neuron 2009, 64:200-212.
50. Stellwagen D., Shatz C.J. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 2002, 33:357-367.
51. Stellwagen D., Shatz C.J., Feller M.B. Dynamics of retinal waves are controlled by cyclic AMP. Neuron 1999, 24:673-685.
52. Sun C., Speer C.M., Wang G.Y., Chapman B., Chalupa L.M. Epibatidine application invitro blocks retinal waves without silencing all retinal ganglion cell action potentials in developing retina of the mouse and ferret. J.Neurophysiol. 2008, 100:3253-3263.
53. Sun C., Warland D.K., Ballesteros J.M., van der List D., Chalupa L.M. Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 2008, 105:13638-13643.
54. Triplett J.W., Owens M.T., Yamada J., Lemke G., Cang J., Stryker M.P., Feldheim D.A. Retinal input instructs alignment of visual topographic maps. Cell 2009, 139:175-185.
55. Wang L., Rangarajan K.V., Lawhn-Heath C.A., Sarnaik R., Wang B.S., Liu X., Cang J. Direction-specific disruption of subcortical visual behavior and receptive fields in mice lacking the beta2 subunit of nicotinic acetylcholine receptor. J.Neurosci. 2009, 29:12909-12918.
56. Weliky M., Katz L.C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus invivo. Science 1999, 285:599-604.
57. White L.E., Coppola D.M., Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 2001, 411:1049-1052.
58. Xu J., Zhu Y., Contractor A., Heinemann S.F. mGluR5 has a critical role in inhibitory learning. J.Neurosci. 2009, 29:3676-3684.
59. Xu H.P., Furman M., Mineur Y.S., Chen H., King S.L., Zenisek D., Zhou Z.J., Butts D.A., Tian N., Picciotto M.R., Crair M.C. An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 2011, 70:1115-1127.
60. Xu J., Cohen B.N., Zhu Y., Dziewczapolski G., Panda S., Lester H.A., Heinemann S.F., Contractor A. Altered activity-rest patterns in mice with a human autosomal-dominant nocturnal frontal lobe epilepsy mutation in the β2 nicotinic receptor. Mol. Psychiatry 2011, 16:1048-1061.
61. Zhang J., Ackman J.B., Xu H.P., Crair M.C. Visual map development depends on the temporal pattern of binocular activity in mice. Nat. Neurosci. 2012, 15:298-307.
62. Zheng J., Lee S., Zhou Z.J. A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves. Nat. Neurosci. 2006, 9:363-371.
63. Zhou Z.J. Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J.Neurosci. 1998, 18:4155-4165.